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Use of MRI to Measure Bronchial Inflammation in Cystic Fibrosis

2019; Radiological Society of North America; Volume: 294; Issue: 1 Linguagem: Inglês

10.1148/radiol.2019192194

1527-1315

Marie-Pierre Revel, Guillaume Chassagnon,

Neonatal Respiratory Health Research

HomeRadiologyVol. 294, No. 1 PreviousNext Reviews and CommentaryFree AccessEditorialUse of MRI to Measure Bronchial Inflammation in Cystic FibrosisMarie-Pierre Revel , Guillaume ChassagnonMarie-Pierre Revel , Guillaume ChassagnonAuthor AffiliationsFrom the Department of Radiology, Cochin Hospital, 27 Rue du Fg Saint Jacques, 75014 Paris, France.Address correspondence to M.P.R. (e-mail: [email protected]).Marie-Pierre Revel Guillaume ChassagnonPublished Online:Oct 29 2019https://doi.org/10.1148/radiol.2019192194MoreSectionsPDF ToolsImage ViewerAdd to favoritesCiteTrack CitationsPermissionsReprints ShareShare onFacebookTwitterLinked In See also the article by Benlala et al in this issue.Dr Marie-Pierre Revel is head of the Cardiothoracic Imaging Department at the University of Paris Cochin Hospital (Paris, France) and past president of the European Society of Thoracic Imaging. Her clinical and scientific work is dedicated to thoracic imaging, specifically pulmonary embolism diagnosis at CT and MRI, lung nodule evaluation, and lung cancer early diagnosis. She heads the lung cancer screening certification program for the European Society of Radiology.Download as PowerPointOpen in Image Viewer Dr Guillaume Chassagnon is an imaging researcher at the University of Paris Cochin Hospital. He received his PhD degree in advanced image analysis from the CentraleSupélec school in Gif-sur-Yvette, France. His research aims to define biomarkers in chronic obstructive and fibrotic lung diseases such as cystic fibrosis and systemic sclerosis. He also has an interest in the development and optimization of lung MRI.Download as PowerPointOpen in Image Viewer Cystic fibrosis (CF) is the most common inherited disease in Europe and the United States, and it affects more than 70 000 individuals in Europe and the United States combined. This recessive autosomal disease is caused by mutations in the cystic fibrosis transmembrane conductance regulator gene that encodes for an epithelial chloride channel involved in ion and fluid transport. The dysfunction of this channel leads to the production of a thickened bronchial mucus and alters the mucociliary clearance, leading to mucoid impactions, bronchial infection and inflammation, and, ultimately, bronchiectasis.Whereas bronchiectasis corresponds to irreversible lesions, inflammatory changes during disease exacerbation (eg, bronchial thickening, mucoid impactions, and consolidation) can be reversible. Quantifying these reversible changes affords an opportunity to evaluate treatment efficacy. Multiple visual scoring methods for assessing lung disease severity in CF have been proposed to date, mainly on the basis of CT. None of these methods has been unanimously adopted. In addition to often being time consuming, these methods require specific training and are associated with inter- and intrareader variability. Moreover, most scoring systems combine the evaluation of reversible and irreversible changes, which will not improve with antibiotics in CF with lung disease exacerbation. Finally, the CT radiation dose limits its repeated use for short-interval assessment, hence the reason why MRI scoring is preferred, particularly in the pediatric population (1).By using lung MRI, the Eichinger score considers bronchiectasis and bronchial wall thickening as a single parameter because MRI spatial resolution is not high enough to differentiate between the two (2). Furthermore, the Eichinger score requires contrast agent administration for the quantification of perfusion defects. However, concerns regarding potential toxicity of gadolinium-based contrast agents and risk of brain accumulation after repeated administration make it preferable to use unenhanced MRI sequences for monitoring response to treatment, even though little is known about the clinical consequences of gadolinium accumulation in the brain (3).In this issue of Radiology, Benlala et al (4) used T2-weighted MRI to monitor inflammation and response to treatment in study participants with CF. Previous reports suggested the use of T2-weighted sequences to depict increased water content observed in lung consolidation, bronchial wall edema, and mucus plugs. The visual scoring of the extent of high T2 signal areas reportedly correlates with biologic markers of inflammation (5). Benlala and colleagues hypothesized that this scoring could be automated and proposed a method for quantifying high T2 signal areas.The authors used a T2-weighted radial fast spin echo (RFSE) sequence with multiple echoes to calculate T2 maps of the lung. Because lung segmentation is not possible on black-blood contrast-enhanced T2-weighted images, Benlala et al (4) also acquired a morphologic three-dimensional ultrashort echo time sequence at the same conditions as the T2-weighted RFSE sequence. The T2-weighted MRI could then be registered to the corresponding morphologic images, to isolate the lungs from the mediastinum and chest wall. Both sequences were performed at free breathing by using prospective respiratory synchronization at end expiration to facilitate image matching. Ultimately, the authors derived a quantitative measure of the amount of high T2 lung signal. The amount of high T2 lung signal was indexed to the total lung volume to account for differences in patient size.Quantification of lung abnormalities on the basis of thresholding is not a new approach. It has been used for emphysema quantification at CT by selecting low-attenuation lung areas with attenuation values less than −950 HU (low-pass filter). More recently, Chassagnon et al (6) quantified high-attenuation structures at CT to evaluate lung disease severity in patients with CF. Indeed, most CF-related lung changes exhibit higher CT attenuation values than normal lung parenchyma, especially bronchial wall thickening and mucus plugging. The drawback is that pulmonary vessels are also included in the CT segmentations. This was not the case at MRI with the approach developed by Benlala et al (4) because of both the black-blood properties of T2-weighted RFSE and the use of a high-pass filter.In addition to the volume of inflammatory lesions, Benlala et al (4) displayed the severity of inflammation by using T2 mapping. T2 mapping has been used for characterization of different fibrotic patterns such as ground glass, reticulations, and honeycombing in fibrotic lung diseases. The median T2 was different between normal and fibrotic areas and among the different components of fibrosis (7). The originality of the method proposed by Benlala and colleagues was to combine T2 mapping with disease segmentation leading to a composite index called T2-weighted volume-intensity product by combining the volume of high T2 areas and their T2 value on T2 mapping.This pilot study included 12 study participants with CF and 10 healthy volunteers. MRI was repeated twice within a 10-minute interval to assess the repeatability in view of the many required steps to obtain the final quantification. As expected, healthy volunteers were found to always have a high T2 lung volume of 0%, whereas patients with cystic fibrosis had a median high T2-weighted lung volume of 4.1% (range, 0.1%–17.0%). The repeatability was excellent (intraclass correlation coefficient, ≥0.97).Six participants with CF referred for pulmonary exacerbations were evaluated before and after treatment by using traditional visual scoring and MRI automated quantification. The conventional visual MRI scores were not different before versus after treatment, whereas the amount of high T2 lung volume was lower after the administration of antibiotics. This strongly suggests the presence of reversible lung changes. Variation of the T2-weighted volume-intensity product was the only parameter correlating with the evolution of pulmonary function tests.What perspectives are opened by this pilot study? This approach could prove useful to monitor disease evolution in non–CF-related bronchiectasis and in response to treatment in cases of exacerbation. Non–CF-related bronchiectasis represents a larger patient group than does CF.Depiction of inflammatory changes as a marker of disease activity could also be of interest in other chronic lung diseases, such as idiopathic pulmonary fibrosis or sarcoidosis. For both conditions, morphologic evaluation alone does not allow for distinguishing between active and cicatricial lesions nor for assessing early response to treatment. Functional imaging can play a major role in the early assessment of the efficacy of released therapies for slowing the fibrotic process in idiopathic pulmonary fibrosis or correcting cystic fibrosis transmembrane conductance regulator protein dysfunction (8) because these therapies are expensive and have potentially undesirable adverse effects.In a Radiology editorial from 2004, Brody (9) cited Jacobsen and colleagues (10), who said, "if bronchocele formation, including mucoid impaction is recognized and treated early, permanent bronchiectasis may be prevented," and Brody mentioned CT as an "essential tool in demonstration of the cure of lung disease in CF." Benlala et al have demonstrated that unenhanced, radiation-free MRI sequences can play this role by quantifying reversible inflammatory changes in CF. Further research will be needed to prove the clinical value of this approach in a larger group of study participants and in other contexts where evaluation of inflammatory lung changes is important.Disclosures of Conflicts of Interest: M.P.R. disclosed no relevant relationships. G.C. disclosed no relevant relationships.References1. Sileo C, Corvol H, Boelle PY, Blondiaux E, Clement A, Ducou Le Pointe H. HRCT and MRI of the lung in children with cystic fibrosis: comparison of different scoring systems. J Cyst Fibros 2014;13(2):198–204. Crossref, Medline, Google Scholar2. Eichinger M, Optazaite DE, Kopp-Schneider A, et al. Morphologic and functional scoring of cystic fibrosis lung disease using MRI. Eur J Radiol 2012;81(6):1321–1329. Crossref, Medline, Google Scholar3. Gulani V, Calamante F, Shellock FG, Kanal E, Reeder SB; International Society for Magnetic Resonance in Medicine. Gadolinium deposition in the brain: summary of evidence and recommendations. Lancet Neurol 2017;16(7):564–570. Crossref, Medline, Google Scholar4. Benlala I, Hocke F, Macey J, et al. Quantification of MRI T2-weighted high signal volume in cystic fibrosis: a pilot study. Radiology 2020;294:186–196. Link, Google Scholar5. Renz DM, Scholz O, Böttcher J, et al. Comparison between magnetic resonance imaging and computed tomography of the lung in patients with cystic fibrosis with regard to clinical, laboratory, and pulmonary functional parameters. Invest Radiol 2015;50(10):733–742. Crossref, Medline, Google Scholar6. Chassagnon G, Martin C, Burgel PR, et al. An automated computed tomography score for the cystic fibrosis lung. Eur Radiol 2018;28(12):5111–5120. Crossref, Medline, Google Scholar7. Buzan MTA, Eichinger M, Kreuter M, et al. T2 mapping of CT remodelling patterns in interstitial lung disease. Eur Radiol 2015;25(11):3167–3174. Crossref, Medline, Google Scholar8. Wainwright CE, Elborn JS, Ramsey BW, et al. Lumacaftor-Ivacaftor in Patients with Cystic Fibrosis Homozygous for Phe508del CFTR. N Engl J Med 2015;373(3):220–231. Crossref, Medline, Google Scholar9. Brody AS. Scoring systems for CT in cystic fibrosis: who cares? Radiology 2004;231(2):296–298. Link, Google Scholar10. Jacobsen LE, Houston CS, Habbick BF, Genereux GP, Howie JL. Cystic fibrosis: a comparison of computed tomography and plain chest radiographs. Can Assoc Radiol J 1986;37(1):17–21. Medline, Google ScholarArticle HistoryReceived: Sept 26 2019Revision requested: Oct 2 2019Revision received: Oct 2 2019Accepted: Oct 4 2019Published online: Oct 29 2019Published in print: Jan 2020 FiguresReferencesRelatedDetailsAccompanying This ArticleQuantification of MRI T2-weighted High Signal Volume in Cystic Fibrosis: A Pilot StudyOct 29 2019RadiologyRecommended Articles Quantification of MRI T2-weighted High Signal Volume in Cystic Fibrosis: A Pilot StudyRadiology2019Volume: 294Issue: 1pp. 186-196Allergic Bronchopulmonary Aspergillosis in Cystic Fibrosis: MR Imaging of Airway Mucus Contrasts as a Tool for DiagnosisRadiology2017Volume: 285Issue: 1pp. 261-269Quantification of Cystic Fibrosis Lung Disease with Radiomics-based CT ScoresRadiology: Cardiothoracic Imaging2020Volume: 2Issue: 6Expanding Applications of Pulmonary MRI in the Clinical Evaluation of Lung Disorders: Fleischner Society Position PaperRadiology2020Volume: 297Issue: 2pp. 286-301Practical Imaging Interpretation in Patients Suspected of Having Idiopathic Pulmonary Fibrosis: Official Recommendations from the Radiology Working Group of the Pulmonary Fibrosis FoundationRadiology: Cardiothoracic Imaging2021Volume: 3Issue: 1See More RSNA Education Exhibits The Role of Thoracic Imaging in Cystic Fibrosis: Correlation with Clinical and Physiological FindingsDigital Posters2019Imaging in Cystic Fibrosis Follow-up: What is the News?Digital Posters2019Mucus Plugs Provide Clues to Respiratory Disease Diagnosis and ManagementDigital Posters2020 RSNA Case Collection Pulmonary manifestations of cystic fibrosisRSNA Case Collection2020Allergic Bronchopulmonary AspergillosisRSNA Case Collection2021Mounier-Kuhn syndromeRSNA Case Collection2020 Vol. 294, No. 1 Metrics Altmetric Score PDF download