Longitudinal Lung Function Assessment of Patients Hospitalized With COVID-19 Using 1H and 129Xe Lung MRI

Abstract

BackgroundMicrovascular abnormalities and impaired gas transfer have been observed in patients with COVID-19. The progression of pulmonary changes in these patients remains unclear.Research QuestionDo patients hospitalized with COVID-19 without evidence of architectural distortion on structural imaging exhibit longitudinal improvements in lung function measured by using 1H and 129Xe MRI between 6 and 52 weeks following hospitalization?Study Design and MethodsPatients who were hospitalized with COVID-19 pneumonia underwent a pulmonary 1H and 129Xe MRI protocol at 6, 12, 25, and 51 weeks following hospital admission in a prospective cohort study between November 2020 and February 2022. The imaging protocol was as follows: 1H ultra-short echo time, contrast-enhanced lung perfusion, 129Xe ventilation, 129Xe diffusion-weighted, and 129Xe spectroscopic imaging of gas exchange.ResultsNine patients were recruited (age 57 ± 14 [median ± interquartile range] years; six of nine patients were male). Patients underwent MRI at 6 (n = 9), 12 (n = 9), 25 (n = 6), and 51 (n = 8) weeks following hospital admission. Patients with signs of interstitial lung damage were excluded. At 6 weeks, patients exhibited impaired 129Xe gas transfer (RBC to membrane fraction), but lung microstructure was not increased (apparent diffusion coefficient and mean acinar airway dimensions). Minor ventilation abnormalities present in four patients were largely resolved in the 6- to 25-week period. At 12 weeks, all patients with lung perfusion data (n = 6) showed an increase in both pulmonary blood volume and flow compared with 6 weeks, although this was not statistically significant. At 12 weeks, significant improvements in 129Xe gas transfer were observed compared with 6-week examinations; however, 129Xe gas transfer remained abnormally low at weeks 12, 25, and 51.Interpretation129Xe gas transfer was impaired up to 1 year following hospitalization in patients who were hospitalized with COVID-19 pneumonia, without evidence of architectural distortion on structural imaging, whereas lung ventilation was normal at 52 weeks. Microvascular abnormalities and impaired gas transfer have been observed in patients with COVID-19. The progression of pulmonary changes in these patients remains unclear. Do patients hospitalized with COVID-19 without evidence of architectural distortion on structural imaging exhibit longitudinal improvements in lung function measured by using 1H and 129Xe MRI between 6 and 52 weeks following hospitalization? Patients who were hospitalized with COVID-19 pneumonia underwent a pulmonary 1H and 129Xe MRI protocol at 6, 12, 25, and 51 weeks following hospital admission in a prospective cohort study between November 2020 and February 2022. The imaging protocol was as follows: 1H ultra-short echo time, contrast-enhanced lung perfusion, 129Xe ventilation, 129Xe diffusion-weighted, and 129Xe spectroscopic imaging of gas exchange. Nine patients were recruited (age 57 ± 14 [median ± interquartile range] years; six of nine patients were male). Patients underwent MRI at 6 (n = 9), 12 (n = 9), 25 (n = 6), and 51 (n = 8) weeks following hospital admission. Patients with signs of interstitial lung damage were excluded. At 6 weeks, patients exhibited impaired 129Xe gas transfer (RBC to membrane fraction), but lung microstructure was not increased (apparent diffusion coefficient and mean acinar airway dimensions). Minor ventilation abnormalities present in four patients were largely resolved in the 6- to 25-week period. At 12 weeks, all patients with lung perfusion data (n = 6) showed an increase in both pulmonary blood volume and flow compared with 6 weeks, although this was not statistically significant. At 12 weeks, significant improvements in 129Xe gas transfer were observed compared with 6-week examinations; however, 129Xe gas transfer remained abnormally low at weeks 12, 25, and 51. 129Xe gas transfer was impaired up to 1 year following hospitalization in patients who were hospitalized with COVID-19 pneumonia, without evidence of architectural distortion on structural imaging, whereas lung ventilation was normal at 52 weeks. FOR EDITORIAL COMMENT, SEE PAGE 572Take-home PointsStudy Question: Do patients hospitalized due to COVID-19 with no evidence of architectural distortion exhibit longitudinal improvements in 129Xe gas transfer to within a normal range between 6 and 52 weeks following hospitalization?Results: At 12 weeks, significant improvements in 129Xe gas transfer were observed compared with 6-week examinations. However, 129Xe gas transfer remained abnormally low at weeks 12, 25, and 51.Interpretation: In a cohort of patients with moderate severity disease, 129Xe gas transfer improved but did not return to within a normal range within 1 year following hospitalization. FOR EDITORIAL COMMENT, SEE PAGE 572 Study Question: Do patients hospitalized due to COVID-19 with no evidence of architectural distortion exhibit longitudinal improvements in 129Xe gas transfer to within a normal range between 6 and 52 weeks following hospitalization? Results: At 12 weeks, significant improvements in 129Xe gas transfer were observed compared with 6-week examinations. However, 129Xe gas transfer remained abnormally low at weeks 12, 25, and 51. Interpretation: In a cohort of patients with moderate severity disease, 129Xe gas transfer improved but did not return to within a normal range within 1 year following hospitalization. In patients hospitalized with pneumonia caused by infection with SARS-CoV-2, the existing literature and clinical experience suggest that there is considerable overlap in clinical presentation with typical pneumonia and ARDS in patients exhibiting hyperinflammation and progressive hypoxemia. However, patients with severe COVID-19 also display evidence of an inflammatory and thrombotic vasculopathy with endothelial dysfunction and excessive blood flow to collapsed lung tissue.1Lang M. Som A. Carey D. et al.Pulmonary vascular manifestations of COVID-19 pneumonia.Radiol Cardiothorac Imaging. 2020; 2e200277Crossref Scopus (97) Google Scholar, 2Loo J. Spittle D.A. Newnham M. COVID-19, immunothrombosis and venous thromboembolism: biological mechanisms.Thorax. 2021; 76: 412-420Crossref PubMed Scopus (184) Google Scholar, 3Attaway A.H. Scheraga R.G. Bhimraj A. Biehl M. Hatipoglu U. Severe Covid-19 pneumonia: pathogenesis and clinical management.BMJ. 2021; 372: n436Crossref PubMed Scopus (185) Google Scholar Abnormal pulmonary vasoregulation has been observed in patients in the acute phase of COVID-191Lang M. Som A. Carey D. et al.Pulmonary vascular manifestations of COVID-19 pneumonia.Radiol Cardiothorac Imaging. 2020; 2e200277Crossref Scopus (97) Google Scholar and may be a pathophysiologic mechanism contributing to the progressive hypoxemia seen in these patients. Abnormalities on chest radiograph or CT scan imaging at 12 weeks following hospitalization due to COVID-19 are present in some patients, particularly those with more severe disease who require ICU treatment.4Robey R.C. Kemp K. Hayton P. et al.Pulmonary sequelae at 4 months after COVID-19 infection: a single-centre experience of a COVID follow-up service.Adv Ther. 2021; 38: 4505-4519Crossref PubMed Scopus (13) Google Scholar However, for patients without radiographic abnormalities, sensitive techniques for monitoring longitudinal change in lung function are needed. Lung MRI with hyperpolarized 129Xe gas allows direct, regionally sensitive measurements of lung ventilation and function, and it is an emerging method that is used both clinically and in clinical research, alongside 1H MRI, to evaluate lung function and abnormalities.5Stewart N.J. Smith L.J. Chan H.F. et al.Lung MRI with hyperpolarised gases: current & future clinical perspectives.Br J Radiol. 2022; 9520210207Crossref Scopus (21) Google Scholar, 6Collier G.J. Eaden J.A. Hughes P.J.C. et al.Dissolved (129) Xe lung MRI with four-echo 3D radial spectroscopic imaging: quantification of regional gas transfer in idiopathic pulmonary fibrosis.Magn Reson Med. 2021; 85: 2622-2633Crossref PubMed Scopus (21) Google Scholar, 7Wielputz M.O. Puderbach M. Kopp-Schneider A. et al.Magnetic resonance imaging detects changes in structure and perfusion, and response to therapy in early cystic fibrosis lung disease.Am J Respir Crit Care Med. 2014; 189: 956-965Crossref PubMed Scopus (203) Google Scholar, 8Ohno Y. Koyama H. Matsumoto K. et al.Dynamic MR perfusion imaging: capability for quantitative assessment of disease extent and prediction of outcome for patients with acute pulmonary thromboembolism.J Magn Reson Imaging. 2010; 31: 1081-1090Crossref PubMed Scopus (36) Google Scholar, 9Thomen R.P. Walkup L.L. Roach D.J. et al.Regional structure-function in cystic fibrosis lung disease using hyperpolarized (129)Xe and ultrashort echo magnetic resonance imaging.Am J Respir Crit Care Med. 2020; 202: 290-292Crossref PubMed Scopus (17) Google Scholar, 10Tafti S. Garrison W.J. Mugler 3rd, J.P. et al.Emphysema index based on hyperpolarized (3)He or (129)Xe diffusion MRI: performance and comparison with quantitative CT and pulmonary function tests.Radiology. 2020; 297: 201-210Crossref PubMed Scopus Google Scholar, et and 129Xe MRI ventilation after in PubMed Google Scholar In 129Xe gas diffusion within the lung MRI and the diffusion coefficient and mean in of the lung microstructure that is sensitive to changes in patients with et hyperpolarized MRI in and with pulmonary Reson Med. Scopus Google Scholar and lung H.F. et microstructure in idiopathic pulmonary assessment at hyperpolarized PubMed Scopus Google Scholar In 129Xe is in the and in the and the 129Xe in these be The of the 129Xe MRI observed in the lung the lung and to the be with magnetic resonance spectroscopic In the of the 129Xe in the to to gas and to gas have been used to gas H. N.J. Chan H.F. M. In and of magnetic Magn Reson 2021; PubMed Scopus Google et hyperpolarized MRI to the regional and to 2021; PubMed Scopus Google Scholar and are sensitive to gas transfer and longitudinal change in and pulmonary vascular N.J. Chan H.F. et magnetic resonance for the longitudinal assessment of changes in gas diffusion in PubMed Scopus Google Scholar, et hyperpolarized (129)Xe MRI to regional gas transfer in idiopathic pulmonary PubMed Scopus Google Scholar, K. M. et of gas in with hyperpolarised 2021; 76: PubMed Scopus Google Scholar has been to with the transfer for G.J. Eaden J.A. Hughes P.J.C. et al.Dissolved (129) Xe lung MRI with four-echo 3D radial spectroscopic imaging: quantification of regional gas transfer in idiopathic pulmonary fibrosis.Magn Reson Med. 2021; 85: 2622-2633Crossref PubMed Scopus (21) Google J. et of hyperpolarized (129) Xe gas transfer PubMed Scopus Google Scholar have in patients with H. Y. et lung gas function of COVID-19 patients by hyperpolarized (129)Xe 2021; PubMed Scopus Google Scholar, M. G.J. et (129)Xe MRI abnormalities in patients months after COVID-19 pneumonia: 2021; PubMed Scopus Google Scholar, G.J. H. et al.Lung abnormalities with hyperpolarized MRI in patients with 2022; PubMed Scopus Google Scholar, et (129)Xe MRI pulmonary and CT vascular abnormalities in with COVID-19 2022; PubMed Scopus Google Scholar in patients with normal chest CT scan imaging but M. G.J. et (129)Xe MRI abnormalities in patients months after COVID-19 pneumonia: 2021; PubMed Scopus Google Scholar In patients with lung abnormalities on CT may be due to an increase of in the interstitial lung However, in the of CT scan abnormalities, that a in may be a sensitive for longitudinal assessment of regional gas abnormalities in patients who have COVID-19 and have normal structural is following COVID-19 in the may be in (129)Xe MRI for with COVID-19 2022; PubMed Scopus Google Scholar and for are for of in is also patients with have abnormalities in lung perfusion or 1H lung MRI is to changes in lung structure and echo imaging of the lung and has with CT scan imaging in the of in patients with S. Y. J. et of for and Magn Reson Imaging. 2020; PubMed Scopus (36) Google Scholar contrast-enhanced 1H lung MRI allows the assessment of lung perfusion, with and in perfusion without the to S. et al.Lung MRI for in pulmonary Magn Reson Imaging. PubMed Scopus Google Scholar and it is for follow-up lung perfusion to have been in both an acute hospitalized with COVID-19 and in patients with who have S. J. A. et may be by an in the 2021; PubMed Scopus Google et al.Lung perfusion in with magnetic resonance imaging Med. 2022; PubMed Scopus Google Scholar The current study used a 1H and 129Xe MRI protocol that hyperpolarized 129Xe imaging sensitive to ventilation, lung microstructure and gas spectroscopic alongside 1H perfusion and lung structural imaging to pathophysiologic changes in patients who been hospitalized with COVID-19 pneumonia the period. The of this was that imaging and pulmonary function of lung function increase to within a normal range the of 1 year in patients without structural abnormalities seen on CT scan or structural Patients underwent up to four follow-up MRI at 6, 12, and 52 weeks following hospitalization. Patients with acute COVID-19 pneumonia and no disease were recruited and November 2020 to February for this prospective cohort to or following 129Xe and 1H lung MRI were at 6, 12, and 52 weeks following COVID-19 Patients were to the following a a or hospitalization with a of pneumonia radiograph or CT scan with COVID-19 of impaired on and no evidence of interstitial lung damage on CT scan or MRI structural imaging at 12 weeks following hospital as by a clinical chest Patients with evidence of interstitial lung damage at 12 weeks following hospital admission were recruited the Lung et the of interstitial lung disease the Lung COVID Study Respir 2021; PubMed Scopus (21) Google Scholar MRI were to all In patients were were to a of 129Xe gas to the or a chest the 129Xe chest were on the as the MRI at and transfer were and these the and transfer coefficient were and as and using Lung S. et Lung for the transfer for Respir J. Scopus Google S. et for for the the Lung Respir J. 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PubMed Scopus Google Scholar spectroscopic imaging of the gas and phase in lung and in blood was by using a 1 of hyperpolarized 129Xe = = with G.J. Eaden J.A. Hughes P.J.C. et al.Dissolved (129) Xe lung MRI with four-echo 3D radial spectroscopic imaging: quantification of regional gas transfer in idiopathic pulmonary fibrosis.Magn Reson Med. 2021; 85: 2622-2633Crossref PubMed Scopus (21) Google Scholar 1H MRI was by using an were with a radial of with prospective on S. 3D ultrashort echo pulmonary Reson Med. PubMed Scopus Google Scholar J. A. 3D quantitative of blood volume and endothelial in Magn Reson Imaging. PubMed Google by and measurements in the of Reson Med. 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At 6 weeks following four of nine patients ventilation was in of nine patients, and gas transfer was the ± of and in of nine patients. At 12 weeks, improvements were seen in lung ventilation and gas However, there was no longitudinal change in gas transfer between 12 and 52 weeks, and 129Xe gas transfer in these patients remained that some of the patients with COVID-19 exhibited abnormalities in 129Xe gas transfer at 12 to 51 weeks following normal lung structural imaging and ventilation, with six of patients the ± of normal and patients at 51 weeks. have gas transfer to the in patients hospitalized due to M. G.J. et (129)Xe MRI abnormalities in patients months after COVID-19 pneumonia: 2021; PubMed Scopus Google Scholar, G.J. H. et al.Lung abnormalities with hyperpolarized MRI in patients with 2022; PubMed Scopus Google Scholar, et (129)Xe MRI pulmonary and CT vascular abnormalities in with COVID-19 2022; PubMed Scopus Google Scholar gas transfer on both the in the lung and the in the a of lung perfusion abnormalities endothelial changes may be the gas transfer seen in patients following COVID-19. not to the those due to in imaging are in with the of between hospital and weeks in H. Y. et lung gas function of COVID-19 patients by hyperpolarized (129)Xe 2021; PubMed Scopus Google Scholar, M. G.J. et (129)Xe MRI abnormalities in patients months after COVID-19 pneumonia: 2021; PubMed Scopus Google Scholar, G.J. H. et al.Lung abnormalities with hyperpolarized MRI in patients with 2022; PubMed Scopus Google Scholar In the current the of data and that these changes are not due to or between and patients in this and did not significant longitudinal change for that the change in was a of changes in both and significant in at was also The changes in are not and are in the of 1 also that changes in gas transfer increased with increased and lung perfusion blood volume and pulmonary blood patients with data an increase in regional pulmonary blood flow and volume between 1 and a perfusion may improvements at 12 weeks, and that may be changes in in these patients. 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Hughes P.J.C. et al.Dissolved (129) Xe lung MRI with four-echo 3D radial spectroscopic imaging: quantification of regional gas transfer in idiopathic pulmonary fibrosis.Magn Reson Med. 2021; 85: 2622-2633Crossref PubMed Scopus (21) Google Scholar in lung microstructure measured using 129Xe G.J. Eaden J.A. Hughes P.J.C. et al.Dissolved (129) Xe lung MRI with four-echo 3D radial spectroscopic imaging: quantification of regional gas transfer in idiopathic pulmonary fibrosis.Magn Reson Med. 2021; 85: 2622-2633Crossref PubMed Scopus (21) Google Scholar in lung M. Eaden J.A. et of lung ventilation in interstitial lung disease (129)Xe and Reson Imaging. PubMed Scopus Google Scholar and in lung Eaden J.A. Hughes P.J.C. et of pulmonary perfusion in idiopathic pulmonary fibrosis with contrast-enhanced perfusion 2021; 76: PubMed Scopus Google Scholar this that there is considerable for lung MRI to longitudinal in patients with signs of interstitial lung it also that perfusion, ventilation, gas and lung microstructure abnormalities may be to the changes within a cohort with structural lung using a 1H and 129Xe protocol in patients with pulmonary fibrosis due to COVID-19 on CT scan imaging is the of an study et the of interstitial lung disease the Lung COVID Study Respir 2021; PubMed Scopus (21) Google Scholar Minor ventilation and were present in this cohort following acute these improved time, is with the of et M. G.J. et (129)Xe MRI abnormalities in patients months after COVID-19 pneumonia: 2021; PubMed Scopus Google Scholar and of et H. Y. et lung gas function of COVID-19 patients by hyperpolarized (129)Xe 2021; PubMed Scopus Google Scholar the current study and the literature suggest it is that impaired lung ventilation is the of following the acute of COVID-19 and that the is not of the The of the current study is the of was largely caused by the of patients for following a hospitalization due to COVID-19 in the of the In not all patients lung perfusion imaging or at all to The recruited with and lung function, as as the used to for 129Xe were at 1 in some between patients in the lung of in this study is that patients who were for the study were due to chest the of the MRI study that in a cohort of patients who were hospitalized with COVID-19 pneumonia of moderate severity who normal CT structural imaging, 129Xe gas transfer improved at 12 weeks but did not return to within a normal range within 1 year following hospitalization. in 129Xe gas transfer were with an increased lung perfusion on and increased abnormalities in 129Xe gas transfer may be a of abnormalities was within a normal range for of patients with data at 51 weeks that 129Xe gas transfer may be a more sensitive of gas in this and that it may be to abnormalities that clinical this to be the follow-up study of patients with an range of lung imaging the and of MRI to follow-up lung in a clinical study was by a a and a to J. M. A. A. was by a The study was by the the was by A. J. S. and K. M. H. for the of an MRI used in this

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