Abstract
Objectives
Rapidly progressive interstitial lung disease (RP-ILD) is a life-threatening form of idiopathic inflammatory myopathy (IIM)-associated interstitial lung disease (ILD). We aimed to assess the combination of 18F-fluorodeoxyglucose (FDG) positron emission tomography-computed tomography (PET/CT) and high-resolution computed tomography (HRCT) for the quantification of IIM-ILD activity and risk stratification for RP-ILD.
Method
Patients with IIM and undergoing 18F-FDG PET/CT were included in this retrospective study. Pulmonary FDG uptake was assessed using the maximum standardized uptake value (SUVlung) and visual score (PET score). HRCT was evaluated using visual analysis (HRCT score). Multivariable logistic regression was used to identify risk factors for RP-ILD.
Results
Seventy-three patients with IIM (17 with RP-ILD, 38 with non-RP-ILD, and 18 without ILD) were included. SUVlung, PET score, and HRCT score were significantly higher in RP-ILD than in non-RP-ILD. Strong positive correlations were observed between SUVlung, PET score, and the HRCT parameters. The area under the curve (AUC) of the PET score to differentiate between RP-ILD and non-RP-ILD (AUC = 0.860) was higher than that of the SUVlung (AUC = 0.802) and HRCT scores (AUC = 0.806). We developed a risk score based on the number of positive risk factors (PET score > 18, HRCT score > 140, and positive anti-melanoma differentiation-associated gene 5 (MDA5) antibody) to differentiate between RP-ILD and non-RP-ILD (AUC = 0.955). Patients with higher risk scores had significantly worse prognoses.
Conclusions
18F-FDG PET/CT is useful for assessing disease activity in patients with IIM-ILD. The combination of PET score, HRCT score, and anti-MDA5 antibody can be used to identify patients at increased risk of RP-ILD and with poor prognoses.
Key Points • 18 F-FDG PET/CT helps to assess the inflammatory burden in patients with IIM-ILD. • Whole-lung FDG uptake assessment (PET score) showed superior performance in discriminating RP-ILD and non-RP-ILD compared with SUV lung and HRCT visual analysis. • The combination of PET score, HRCT score, and anti-MDA5 antibody can identify patients at increased risk of RP-ILD and with poor prognoses. |
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Hervier B, Uzunhan Y (2019) Inflammatory myopathy-related interstitial lung disease: from pathophysiology to treatment. Front Med (Lausanne) 6:326. https://doi.org/10.3389/fmed.2019.00326
Wu W, Guo L, Fu Y et al (2021) Interstitial lung disease in anti-MDA5 positive dermatomyositis. Clin Rev Allergy Immunol 60:293–304. https://doi.org/10.1007/s12016-020-08822-5
Hozumi H, Enomoto N, Kono M et al (2015) Prognostic significance of anti-aminoacyl-tRNA synthetase antibodies in polymyositis/dermatomyositis-associated interstitial lung disease: a retrospective case control study. PLoS ONE 10:e0120313. https://doi.org/10.1371/journal.pone.0120313
Zou J, Guo Q, Chi J, Wu H, Bao C (2015) HRCT score and serum ferritin level are factors associated to the 1-year mortality of acute interstitial lung disease in clinically amyopathic dermatomyositis patients. Clin Rheumatol 34:707–714. https://doi.org/10.1007/s10067-015-2866-5
Zuo Y, Ye L, Liu M et al (2020) Clinical significance of radiological patterns of HRCT and their association with macrophage activation in dermatomyositis. Rheumatology (Oxford) 59:2829–2837. https://doi.org/10.1093/rheumatology/keaa034
Nobashi T, Kubo T, Nakamoto Y et al (2016) 18F-FDG uptake in less affected lung field provides prognostic stratification in patients with interstitial lung disease. J Nucl Med 57:1899–1904. https://doi.org/10.2967/jnumed.116.174946
Liang J, Cao H, Liu Y et al (2021) The lungs were on fire: a pilot study of (18)F-FDG PET/CT in idiopathic-inflammatory-myopathy-related interstitial lung disease. Arthritis Res Ther 23:198. https://doi.org/10.1186/s13075-021-02578-9
Uehara T, Takeno M, Hama M et al (2016) Deep-inspiration breath-hold 18F-FDG-PET/CT is useful for assessment of connective tissue disease associated interstitial pneumonia. Mod Rheumatol 26:121–127. https://doi.org/10.3109/14397595.2015.1054099
Win T, Screaton NJ, Porter JC et al (2018) Pulmonary (18)F-FDG uptake helps refine current risk stratification in idiopathic pulmonary fibrosis (IPF). Eur J Nucl Med Mol Imaging 45:806–815. https://doi.org/10.1007/s00259-017-3917-8
Fraioli F, Lyasheva M, Porter JC et al (2019) Synergistic application of pulmonary (18)F-FDG PET/HRCT and computer-based CT analysis with conventional severity measures to refine current risk stratification in idiopathic pulmonary fibrosis (IPF). Eur J Nucl Med Mol Imaging 46:2023–2031. https://doi.org/10.1007/s00259-019-04386-5
Bohan A, Peter JB (1975) Polymyositis and dermatomyositis (first of two parts). N Engl J Med 292:344–347. https://doi.org/10.1056/NEJM197502132920706
Sontheimer RD (2002) Would a new name hasten the acceptance of amyopathic dermatomyositis (dermatomyositis sine myositis) as a distinctive subset within the idiopathic inflammatory dermatomyopathies spectrum of clinical illness? J Am Acad Dermatol 46:626–636. https://doi.org/10.1067/mjd.2002.120621
Travis WD, Costabel U, Hansell DM et al (2013) 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 188:733–748. https://doi.org/10.1164/rccm.201308-1483ST
Akira M, Hamada H, Sakatani M, Kobayashi C, Nishioka M, Yamamoto S (1997) CT findings during phase of accelerated deterioration in patients with idiopathic pulmonary fibrosis. AJR Am J Roentgenol 168:79–83. https://doi.org/10.2214/ajr.168.1.8976924
Boellaard R, Delgado-Bolton R, Oyen WJ et al (2015) FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging 42:328–354. https://doi.org/10.1007/s00259-014-2961-x
Barrington SF, Qian W, Somer EJ et al (2010) Concordance between four European centres of PET reporting criteria designed for use in multicentre trials in Hodgkin lymphoma. Eur J Nucl Med Mol Imaging 37:1824–1833. https://doi.org/10.1007/s00259-010-1490-5
Hansell DM, Bankier AA, MacMahon H, McLoud TC, Muller NL, Remy J (2008) Fleischner Society: glossary of terms for thoracic imaging. Radiology 246:697–722. https://doi.org/10.1148/radiol.2462070712
Ichikado K, Suga M, Muller NL et al (2002) Acute interstitial pneumonia: comparison of high-resolution computed tomography findings between survivors and nonsurvivors. Am J Respir Crit Care Med 165:1551–1556. https://doi.org/10.1164/rccm.2106157
Lian X, Zou J, Guo Q et al (2020) Mortality risk prediction in amyopathic dermatomyositis associated with interstitial lung disease: the FLAIR model. Chest 158:1535–1545. https://doi.org/10.1016/j.chest.2020.04.057
Ichikado K, Suga M, Muranaka H et al (2006) Prediction of prognosis for acute respiratory distress syndrome with thin-section CT: validation in 44 cases. Radiology 238:321–329. https://doi.org/10.1148/radiol.2373041515
Kurasawa K, Arai S, Namiki Y et al (2018) Tofacitinib for refractory interstitial lung diseases in anti-melanoma differentiation-associated 5 gene antibody-positive dermatomyositis. Rheumatology (Oxford) 57:2114–2119. https://doi.org/10.1093/rheumatology/key188
Jacquelin V, Mekinian A, Brillet PY et al (2016) FDG-PET/CT in the prediction of pulmonary function improvement in nonspecific interstitial pneumonia. A Pilot Study. Eur J Radiol 85:2200–2205. https://doi.org/10.1016/j.ejrad.2016.10.001
Justet A, Laurent-Bellue A, Thabut G et al (2017) [(18)F]FDG PET/CT predicts progression-free survival in patients with idiopathic pulmonary fibrosis. Respir Res 18:74. https://doi.org/10.1186/s12931-017-0556-3
Ledoult E, Morelle M, Soussan M et al (2021) (18)F-FDG positron emission tomography scanning in systemic sclerosis-associated interstitial lung disease: a pilot study. Arthritis Res Ther 23:76. https://doi.org/10.1186/s13075-021-02460-8
Yamanaka Y, Baba T, Hagiwara E et al (2018) Radiological images of interstitial pneumonia in mixed connective tissue disease compared with scleroderma and polymyositis/dermatomyositis. Eur J Radiol 107:26–32. https://doi.org/10.1016/j.ejrad.2018.08.005
Tanizawa K, Handa T, Nakashima R et al (2013) The prognostic value of HRCT in myositis-associated interstitial lung disease. Respir Med 107:745–752. https://doi.org/10.1016/j.rmed.2013.01.014
El-Chemaly S, Malide D, Yao J et al (2013) Glucose transporter-1 distribution in fibrotic lung disease: association with [(1)(8)F]-2-fluoro-2-deoxyglucose-PET scan uptake, inflammation, and neovascularization. Chest 143:1685–1691. https://doi.org/10.1378/chest.12-1359
Xu W, Wu W, Zhang D et al (2021) A novel CT scoring method predicts the prognosis of interstitial lung disease associated with anti-MDA5 positive dermatomyositis. Sci Rep 11:17070. https://doi.org/10.1038/s41598-021-96292-w
Win T, Thomas BA, Lambrou T et al (2014) Areas of normal pulmonary parenchyma on HRCT exhibit increased FDG PET signal in IPF patients. Eur J Nucl Med Mol Imaging 41:337–342. https://doi.org/10.1007/s00259-013-2514-8
Sato S, Hoshino K, Satoh T et al (2009) RNA helicase encoded by melanoma differentiation-associated gene 5 is a major autoantigen in patients with clinically amyopathic dermatomyositis: association with rapidly progressive interstitial lung disease. Arthritis Rheum 60:2193–2200. https://doi.org/10.1002/art.24621
Waseda Y, Johkoh T, Egashira R et al (2016) Antisynthetase syndrome: pulmonary computed tomography findings of adult patients with antibodies to aminoacyl-tRNA synthetases. Eur J Radiol 85:1421–1426. https://doi.org/10.1016/j.ejrad.2016.05.012
Debray MP, Borie R, Revel MP et al (2015) Interstitial lung disease in anti-synthetase syndrome: initial and follow-up CT findings. Eur J Radiol 84:516–523. https://doi.org/10.1016/j.ejrad.2014.11.026
Tanizawa K, Handa T, Nakashima R et al (2011) HRCT features of interstitial lung disease in dermatomyositis with anti-CADM-140 antibody. Respir Med 105:1380–1387. https://doi.org/10.1016/j.rmed.2011.05.006
Cao H, Liang J, Xu D et al (2021) Radiological characteristics of patients with anti-MDA5-antibody-positive dermatomyositis in (18)F-FDG PET/CT: a pilot study. Front Med (Lausanne) 8:779272. https://doi.org/10.3389/fmed.2021.779272
Acknowledgements
We would like to thank Chang Yi, Xincong Shi, Ganhua Luo, Zhaorong Lu, Fuhua Wen, Dake Zhang, and Renbo Wu for technical assistance.
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Xiangsong Zhang and Kejing Tang contributed to the conception and design of the study; Yuying Zhang, Bing Zhang, Qiao He, and Yali Long contributed to data collection and analysis. Zhifeng Chen and Xiangsong Zhang performed image interpretation and analysis. Yuying Zhang drafted the manuscript. Zhifeng Chen and Xiangsong Zhang revised the manuscript critically. All authors read and approved the final manuscript.
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The study protocol was approved by the Ethics Committee of FAHSYSU and was conducted in accordance with the principles of the Declaration of Helsinki.
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Zhang, Y., Chen, Z., Long, Y. et al. 18F-FDG PET/CT and HRCT: a combined tool for risk stratification in idiopathic inflammatory myopathy-associated interstitial lung disease. Clin Rheumatol 41, 3095–3105 (2022). https://doi.org/10.1007/s10067-022-06239-3
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DOI: https://doi.org/10.1007/s10067-022-06239-3