Approach to Pulmonary Nodules in Connective Tissue Disease

Brian Gaffney; David J. Murphy

doi:10.1055/s-0044-1782656

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2024; 45(03): 316-328
DOI: 10.1055/s-0044-1782656

Review Article

Approach to Pulmonary Nodules in Connective Tissue Disease

Authors

Brian Gaffney

¹Department of Radiology, St Vincent's University Hospital, Dublin, Ireland
David J. Murphy

¹Department of Radiology, St Vincent's University Hospital, Dublin, Ireland

²School of Medicine, University College, Dublin, Ireland

Abstract

The assessment of pulmonary nodules is a common and often challenging clinical scenario. This evaluation becomes even more complex in patients with connective tissue diseases (CTDs), as a range of disease-related factors must also be taken into account. These diseases are characterized by immune-mediated chronic inflammation, leading to tissue damage, collagen deposition, and subsequent organ dysfunction. A thorough examination of nodule features in these patients is required, incorporating anatomic and functional information, along with patient demographics, clinical factors, and disease-specific knowledge. This integrated approach is vital for effective risk stratification and precise diagnosis. This review article addresses specific CTD-related factors that should be taken into account when evaluating pulmonary nodules in this patient group.

Keywords

nodule - rheumatoid - nodule; rheumatic - computed tomography - positron emission tomography

Full Text

References

References
1 Hansell DM, Bankier AA, MacMahon H, McLoud TC, Müller NL, Remy J. Fleischner Society: glossary of terms for thoracic imaging. Radiology 2008; 246 (03) 697-722
2 Larici AR, Farchione A, Franchi P. et al. Lung nodules: size still matters. Eur Respir Rev 2017; 26 (146) 170025
3 Gould MK, Tang T, Liu I-LA. et al. Recent trends in the identification of incidental pulmonary nodules. Am J Respir Crit Care Med 2015; 192 (10) 1208-1214
4 Mazzone PJ, Lam L. Evaluating the patient with a pulmonary nodule: a review. JAMA 2022; 327 (03) 264-273
5 McWilliams A, Tammemagi MC, Mayo JR. et al. Probability of cancer in pulmonary nodules detected on first screening CT. N Engl J Med 2013; 369 (10) 910-919
6 Wang S, Xu F, Wang Y. et al. Relevant risk factor and follow-up of lung nodules in physical examination with low-dose CT screening. Iran J Public Health 2023; 52 (02) 350-359
7 MacMahon H, Naidich DP, Goo JM. et al. Guidelines for management of incidental pulmonary nodules detected on CT images: from the Fleischner Society 2017. Radiology 2017; 284 (01) 228-243
8 Bankier AA, MacMahon H, Goo JM, Rubin GD, Schaefer-Prokop CM, Naidich DP. Recommendations for measuring pulmonary nodules at CT: a statement from the Fleischner Society. Radiology 2017; 285 (02) 584-600
9 de Koning HJ, van der Aalst CM, de Jong PA. et al. Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl J Med 2020; 382 (06) 503-513
10 Callister MEJ, Baldwin DR, Akram AR. et al. British Thoracic Society Pulmonary Nodule Guideline Development Group, British Thoracic Society Standards of Care Committee. British Thoracic Society guidelines for the investigation and management of pulmonary nodules. Thorax 2015; 70 (Suppl. 02) ii1-ii54
11 Devaraj A, van Ginneken B, Nair A, Baldwin D. Use of volumetry for lung nodule management: theory and practice. Radiology 2017; 284 (03) 630-644
12 Aberle DR, Adams AM, Berg CD. et al. National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011; 365 (05) 395-409
13 Horeweg N, van Rosmalen J, Heuvelmans MA. et al. Lung cancer probability in patients with CT-detected pulmonary nodules: a prespecified analysis of data from the NELSON trial of low-dose CT screening. Lancet Oncol 2014; 15 (12) 1332-1341
14 Gaerte SC, Meyer CA, Winer-Muram HT, Tarver RD, Conces Jr DJ. Fat-containing lesions of the chest. Radiographics 2002; 22 Spec No: S61-S78
15 Truong MT, Ko JP, Rossi SE. et al. Update in the evaluation of the solitary pulmonary nodule. Radiographics 2014; 34 (06) 1658-1679
16 Nasrullah A, Fadl S, Ahuja J, Xu H, Kicska G. Radiographic signs and patterns in interstitial lung disease. Semin Roentgenol 2019; 54 (01) 66-72
17 Fletcher JW, Kymes SM, Gould M. et al. VA SNAP Cooperative Studies Group. A comparison of the diagnostic accuracy of 18F-FDG PET and CT in the characterization of solitary pulmonary nodules. J Nucl Med 2008; 49 (02) 179-185
18 Herder GJ, van Tinteren H, Golding RP. et al. Clinical prediction model to characterize pulmonary nodules: validation and added value of 18F-fluorodeoxyglucose positron emission tomography. Chest 2005; 128 (04) 2490-2496
19 Burris NS, Johnson KM, Larson PEZ. et al. Detection of small pulmonary nodules with ultrashort echo time sequences in oncology patients by using a PET/MR system. Radiology 2016; 278 (01) 239-246
20 Wu L-M, Xu J-R, Hua J. et al. Can diffusion-weighted imaging be used as a reliable sequence in the detection of malignant pulmonary nodules and masses?. Magn Reson Imaging 2013; 31 (02) 235-246
21 Palmucci S, Galioto F, Fazio G. et al. Clinical and radiological features of lung disorders related to connective-tissue diseases: a pictorial essay. Insights Imaging 2022; 13 (01) 108
22 Spagnolo P, Cordier J-F, Cottin V. Connective tissue diseases, multimorbidity and the ageing lung. Eur Respir J 2016; 47 (05) 1535-1558
23 Ahuja J, Arora D, Kanne JP, Henry TS, Godwin JD. Imaging of pulmonary manifestations of connective tissue diseases. Radiol Clin North Am 2016; 54 (06) 1015-1031
24 Myasoedova E, Crowson CS, Kremers HM, Therneau TM, Gabriel SE. Is the incidence of rheumatoid arthritis rising?: results from Olmsted County, Minnesota, 1955-2007. Arthritis Rheum 2010; 62 (06) 1576-1582
25 de Lauretis A, Veeraraghavan S, Renzoni E. Review series: Aspects of interstitial lung disease: connective tissue disease-associated interstitial lung disease: how does it differ from IPF? How should the clinical approach differ?. Chron Respir Dis 2011; 8 (01) 53-82
26 Messina R, Guggino G, Benfante A, Scichilone N. Interstitial lung disease in elderly rheumatoid arthritis patients. Drugs Aging 2020; 37 (01) 11-18
27 Bilgici A, Ulusoy H, Kuru O, Celenk C, Unsal M, Danaci M. Pulmonary involvement in rheumatoid arthritis. Rheumatol Int 2005; 25 (06) 429-435
28 Demoruelle MK, Weisman MH, Simonian PL. et al. Brief report: airways abnormalities and rheumatoid arthritis-related autoantibodies in subjects without arthritis: early injury or initiating site of autoimmunity?. Arthritis Rheum 2012; 64 (06) 1756-1761
29 Wilsher M, Voight L, Milne D. et al. Prevalence of airway and parenchymal abnormalities in newly diagnosed rheumatoid arthritis. Respir Med 2012; 106 (10) 1441-1446
30 Cottin V, Hirani NA, Hotchkin DL. et al. Presentation, diagnosis and clinical course of the spectrum of progressive-fibrosing interstitial lung diseases. Eur Respir Rev 2018; 27 (150) 180076
31 Shaw M, Collins BF, Ho LA, Raghu G. Rheumatoid arthritis-associated lung disease. Eur Respir Rev 2015; 24 (135) 1-16
32 Yousem SA, Colby TV, Carrington CB. Lung biopsy in rheumatoid arthritis. Am Rev Respir Dis 1985; 131 (05) 770-777
33 Kumar V, Abbas AK, Aster JC. eds. Robbins & Cotran Pathologic Basis of Disease. 10th ed. Philadelphia, PA:: Elsevier; 2021
34 Nyhäll-Wåhlin B-M, Turesson C, Jacobsson LTH. et al. The presence of rheumatoid nodules at early rheumatoid arthritis diagnosis is a sign of extra-articular disease and predicts radiographic progression of joint destruction over 5 years. Scand J Rheumatol 2011; 40 (02) 81-87
35 Tilstra JS, Lienesch DW. Rheumatoid nodules. Dermatol Clin 2015; 33 (03) 361-371
36 Koslow M, Young JR, Yi ES. et al. Rheumatoid pulmonary nodules: clinical and imaging features compared with malignancy. Eur Radiol 2019; 29 (04) 1684-1692
37 Sharma A, Kasetty A, Kumar A. Rheumatoid lung nodules with “feeding-vessel” sign. Clin Rheumatol 2021; 40 (04) 1645-1647
38 Chansakul T, Dellaripa PF, Doyle TJ, Madan R. Intra-thoracic rheumatoid arthritis: Imaging spectrum of typical findings and treatment related complications. Eur J Radiol 2015; 84 (10) 1981-1991
39 van Ede A, den Broeder A, Wagenaar M, van Riel P, Creemers MCW. Etanercept-related extensive pulmonary nodulosis in a patient with rheumatoid arthritis. J Rheumatol 2007; 34 (07) 1590-1592
40 Toussirot E, Berthelot JM, Pertuiset E. et al. Pulmonary nodulosis and aseptic granulomatous lung disease occurring in patients with rheumatoid arthritis receiving tumor necrosis factor-alpha-blocking agent: a case series. J Rheumatol 2009; 36 (11) 2421-2427
41 Karadeniz H, Cindil E, Babaoğlu H. et al Treatment with biologic DMARDs may not adversely affect lung nodules in rheumatoid arthritis patients. Eur J Rheumatol 2022; 275-281
42 León-Sierra LP, Cajas-Santana LJ, Torres-Saavedra FA. Cavitating pulmonary nodule in rheumatoid arthritis: a case report. Rev Colomb Reumatol Engl Ed 2018; 25 (02) 146-148
43 Wickrematilake G. Complicated rheumatoid nodules in lung. Case Rep Rheumatol 2020; 2020: 6627244
44 Denton CP, Khanna D. Systemic sclerosis. Lancet 2017; 390 (10103): 1685-1699
45 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) 1581-1586
46 Solomon JJ, Olson AL, Fischer A, Bull T, Brown KK, Raghu G. Scleroderma lung disease. Eur Respir Rev 2013; 22 (127) 6-19
47 Li JC, Tadros S, Rosser F, Torok KS. Pulmonary nodules in juvenile systemic sclerosis: a case-series from the National Registry for Childhood Onset Scleroderma (NRCOS). Diagnostics (Basel) 2023; 13 (12) 2103
48 Kim EA, Johkoh T, Lee KS. et al. Interstitial pneumonia in progressive systemic sclerosis: serial high-resolution CT findings with functional correlation. J Comput Assist Tomogr 2001; 25 (05) 757-763
49 Remy-Jardin M, Remy J, Wallaert B, Bataille D, Hatron PY. Pulmonary involvement in progressive systemic sclerosis: sequential evaluation with CT, pulmonary function tests, and bronchoalveolar lavage. Radiology 1993; 188 (02) 499-506
50 Bowman SJ, Ibrahim GH, Holmes G, Hamburger J, Ainsworth JR. Estimating the prevalence among Caucasian women of primary Sjögren's syndrome in two general practices in Birmingham, UK. Scand J Rheumatol 2004; 33 (01) 39-43
51 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 (04) 475-487
52 Ramos-Casals M, Font J, García-Carrasco M. et al. Primary Sjögren syndrome: hematologic patterns of disease expression. Medicine (Baltimore) 2002; 81 (04) 281-292
53 Flament T, Bigot A, Chaigne B, Henique H, Diot E, Marchand-Adam S. Pulmonary manifestations of Sjögren's syndrome. Eur Respir Rev 2016; 25 (140) 110-123
54 Casal Moura M, Navin PJ, Johnson GB. et al. Pulmonary nodules in patients with primary Sjögren's syndrome: causes, clinico-radiologic features, and outcomes. Respir Med 2020; 174: 106200
55 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
56 Koyama M, Johkoh T, Honda O. et al. Pulmonary involvement in primary Sjögren's syndrome: spectrum of pulmonary abnormalities and computed tomography findings in 60 patients. J Thorac Imaging 2001; 16 (04) 290-296
57 Schaefer-Prokop C, Elicker BM. Pulmonary manifestations of systemic diseases. In: Hodler J, Kubik-Huch RA, Von-Schulthess GK. eds. Diseases of the Chest, Breast, Heart and Vessels 2019–2022. Cham: Springer International Publishing; 2019: 127-138 . Available at: http://link.springer.com/10.1007/978-3-030-11149-6_11 Accessed January 20, 2024
58 Kassan SS, Thomas TL, Moutsopoulos HM. et al. Increased risk of lymphoma in sicca syndrome. Ann Intern Med 1978; 89 (06) 888-892
59 Hare SS, Souza CA, Bain G. et al. The radiological spectrum of pulmonary lymphoproliferative disease. Br J Radiol 2012; 85 (1015) 848-864
60 Voulgarelis M, Ziakas PD, Papageorgiou A, Baimpa E, Tzioufas AG, Moutsopoulos HM. Prognosis and outcome of non-Hodgkin lymphoma in primary Sjögren syndrome. Medicine (Baltimore) 2012; 91 (01) 1-9
61 Rodallec M, Guermazi A, Brice P. et al. Imaging of MALT lymphomas. Eur Radiol 2002; 12 (02) 348-356
62 Keraen J, Blanc E, Besson FL. et al. Usefulness of ¹⁸F-labeled fluorodeoxyglucose-positron emission tomography for the diagnosis of lymphoma in primary Sjögren's syndrome. Arthritis Rheumatol 2019; 71 (07) 1147-1157
63 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 (06) 776-781
64 Baqir M, Lowe V, Yi ES, Ryu JH. 18F-FDG PET scanning in pulmonary amyloidosis. J Nucl Med 2014; 55 (04) 565-568
65 Prakash UBS. Respiratory complications in mixed connective tissue disease. Clin Chest Med 1998; 19 (04) 733-746 , ix
66 Gunnarsson R, Hetlevik SO, Lilleby V, Molberg Ø. Mixed connective tissue disease. Best Pract Res Clin Rheumatol 2016; 30 (01) 95-111
67 Sullivan WD, Hurst DJ, Harmon CE. et al. A prospective evaluation emphasizing pulmonary involvement in patients with mixed connective tissue disease. Medicine (Baltimore) 1984; 63 (02) 92-107
68 Bodolay E, Szekanecz Z, Dévényi K. et al. Evaluation of interstitial lung disease in mixed connective tissue disease (MCTD). Rheumatology (Oxford) 2005; 44 (05) 656-661
69 Lota HK. Interstitial lung disease in patients with mixed connective tissue disease. Thorax 2013; 68: 186
70 Lynch DA. Lung disease related to collagen vascular disease. J Thorac Imaging 2009; 24 (04) 299-309
71 Kozuka T, Johkoh T, Honda O. et al. Pulmonary involvement in mixed connective tissue disease: high-resolution CT findings in 41 patients. J Thorac Imaging 2001; 16 (02) 94-98
72 Palmucci S, Di Mari A, Cancemi G. et al. Clinical and radiological features of interstitial lung diseases associated with polymyositis and dermatomyositis. Medicina (Kaunas) 2022; 58 (12) 1757
73 Svensson J, Arkema EV, Lundberg IE, Holmqvist M. Incidence and prevalence of idiopathic inflammatory myopathies in Sweden: a nationwide population-based study. Rheumatology (Oxford) 2017; 56 (05) 802-810
74 Arakawa H, Yamada H, Kurihara Y. et al. Nonspecific interstitial pneumonia associated with polymyositis and dermatomyositis: serial high-resolution CT findings and functional correlation. Chest 2003; 123 (04) 1096-1103
75 Liu Y, Xu L, Wu H. et al. Characteristics and predictors of malignancy in dermatomyositis: analysis of 239 patients from northern China. Oncol Lett 2018; 16 (05) 5960-5968
76 Fujita J, Tokuda M, Bandoh S. et al. Primary lung cancer associated with polymyositis/dermatomyositis, with a review of the literature. Rheumatol Int 2001; 20 (02) 81-84
77 Debray M-P, Borie R, Revel M-P. et al. Interstitial lung disease in anti-synthetase syndrome: initial and follow-up CT findings. Eur J Radiol 2015; 84 (03) 516-523
78 McCarty DJ, Manzi S, Medsger Jr TA, Ramsey-Goldman R, LaPorte RE, Kwoh CK. Incidence of systemic lupus erythematosus. Race and gender differences. Arthritis Rheum 1995; 38 (09) 1260-1270
79 Hannah JR, D'Cruz DP. Pulmonary complications of systemic lupus erythematosus. Semin Respir Crit Care Med 2019; 40 (02) 227-234
80 Gould DM, Daves ML. Roentgenologic findings in systemic lupus erythematosus; an analysis of 100 cases. J Chronic Dis 1955; 2 (02) 136-145
81 Webb WR, Gamsu G. Cavitary pulmonary nodules with systemic lupus erythematosus: differential diagnosis. AJR Am J Roentgenol 1981; 136 (01) 27-31
82 Tamai H, Nishina N, Takeuchi T. Pulmonary vein vasculitis presenting as multiple pulmonary nodules in a patient with systemic lupus erythematosus. J Rheumatol 2019; 46 (03) 323-324
83 Willemink MJ, Persson M, Pourmorteza A, Pelc NJ, Fleischmann D. Photon-counting CT: technical principles and clinical prospects. Radiology 2018; 289 (02) 293-312
84 Aerts HJWL, Velazquez ER, Leijenaar RTH. et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 2014; 5 (01) 4006
85 Ardila D, Kiraly AP, Bharadwaj S. et al. End-to-end lung cancer screening with three-dimensional deep learning on low-dose chest computed tomography. Nat Med 2019; 25 (06) 954-961
86 Ma J, Wang Q, Ren Y, Hu H, Zhao J. . Automatic lung nodule classification with radiomics approach,” Proc. SPIE 9789, Medical Imaging 2016: PACS and Imaging Informatics: Next Generation and Innovations, 978906 (5 April 2016); Available at: https://doi.org/10.1117/12.2220768 . Accesssed March, 2024