Post-Acute Sequelae of COVID-19 Pneumonia: Six-month Chest CT Follow-up
Damiano Caruso, Gisella Guido, Marta Zerunian, Tiziano Polidori, Elena Lucertini, Francesco Pucciarelli, Michela Polici, Carlotta Rucci, Benedetta Bracci, Matteo Nicolai, Antonio Cremona, Chiara De Dominicis, Andrea Laghi, Damiano Caruso, Gisella Guido, Marta Zerunian, Tiziano Polidori, Elena Lucertini, Francesco Pucciarelli, Michela Polici, Carlotta Rucci, Benedetta Bracci, Matteo Nicolai, Antonio Cremona, Chiara De Dominicis, Andrea Laghi
Abstract
Background The long-term post-acute pulmonary sequelae of COVID-19 remain unknown. Purpose To evaluate lung injury in patients affected by COVID-19 pneumonia at the 6-month follow-up CT examination compared with the baseline chest CT examination. Materials and Methods From March 19, 2020, to May 24, 2020, patients with moderate to severe COVID-19 pneumonia who had undergone baseline chest CT were prospectively enrolled at their 6-month follow-up. The CT qualitative findings, semiquantitative Lung Severity Score (LSS), and the well-aerated lung volume at quantitative chest CT (QCCT) analysis were analyzed. The performance of the baseline LSS and QCCT findings for predicting fibrosis-like changes (reticular pattern and/or honeycombing) at the 6-month follow-up chest CT examination was tested by using receiver operating characteristic curves. Univariable and multivariable logistic regression analyses were used to test clinical and radiologic features that were predictive of fibrosis-like changes. The multivariable analysis was performed with clinical parameters alone (clinical model), radiologic parameters alone (radiologic model), and the combination of clinical and radiologic parameters (combined model). Results One hundred eighteen patients who had undergone baseline chest CT and agreed to undergo follow-up chest CT at 6 months were included in the study (62 women; mean age, 65 years ± 12 [standard deviation]). At follow-up chest CT, 85 of 118 (72%) patients showed fibrosis-like changes and 49 of 118 (42%) showed ground-glass opacities. The baseline LSS (>14) and QCCT findings (≤3.75 L and ≤80%) showed excellent performance for predicting fibrosis-like changes at follow-up chest CT. In the multivariable analysis, the areas under the curve were 0.89 (95% CI: 0.77, 0.96) for the clinical model, 0.81 (95% CI: 0.68, 0.9) for the radiologic model, and 0.92 (95% CI: 0.81, 0.98) for the combined model. Conclusion At 6-month follow-up chest CT, 72% of patients showed late sequelae, in particular fibrosis-like changes. The baseline Lung Severity Score and the well-aerated lung volume at quantitative chest CT (QCCT) analysis showed excellent performance for predicting fibrosis-like changes at the 6-month chest CT (area under the curve, >0.88). Male sex, cough, lymphocytosis, and the well-aerated lung volume at QCCT analysis were significant predictors of fibrosis-like changes at 6 months, demonstrating an inverse correlation (area under the curve, 0.92). © RSNA, 2021 See also the editorial by Wells and Devaraj in this issue.
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References
- Naming the coronavirus disease (COVID-19) and the virus that causes it. 2020. . Published 2020.
- Caruso D, Zerunian M, Polici M, Pucciarelli F, Polidori T, Rucci C, Guido G, Bracci B, De Dominicis C, Laghi A. Chest CT Features of COVID-19 in Rome, Italy. Radiology 2020;296(2):E79–e85. 10.1148/radiol.2020201237
- Huang L, Han R, Ai T, Yu P, Kang H, Tao Q, Xia L. Serial quantitative chest ct assessment of covid-19: Deep-learning approach. Radiology: Cardiothoracic Imaging 2020;2(2):e200075.
- Caruso D, Polici M, Zerunian M, Pucciarelli F, Polidori T, Guido G, Rucci C, Bracci B, Muscogiuri E, De Dominicis C, Laghi A. Quantitative Chest CT analysis in discriminating COVID-19 from non-COVID-19 patients. Radiol Med 2020. 10.1007/s11547-020-01291-y
- Shen C, Yu N, Cai S, Zhou J, Sheng J, Liu K, Zhou H, Guo Y, Niu G. Quantitative computed tomography analysis for stratifying the severity of Coronavirus Disease 2019. J Pharm Anal 2020;10(2):123–129. 10.1016/j.jpha.2020.03.004
- Chung M, Bernheim A, Mei X, Zhang N, Huang M, Zeng X, Cui J, Xu W, Yang Y, Fayad ZA, Jacobi A, Li K, Li S, Shan H. CT Imaging Features of 2019 Novel Coronavirus (2019-nCoV). Radiology 2020;295(1):202–207. 10.1148/radiol.2020200230
- Zhan J, Li H, Yu H, Liu X, Zeng X, Peng D, Zhang W. 2019 novel coronavirus (COVID-19) pneumonia: CT manifestations and pattern of evolution in 110 patients in Jiangxi, China. Eur Radiol 2020. 10.1007/s00330-020-07201-0
- Caruso D, Polidori T, Guido G, Nicolai M, Bracci B, Cremona A, Zerunian M, Polici M, Pucciarelli F, Rucci C, Dominicis C, Girolamo MD, Argento G, Sergi D, Laghi A. Typical and atypical COVID-19 computed tomography findings. World J Clin Cases 2020;8(15):3177–3187. 10.12998/wjcc.v8.i15.3177
- Tabatabaei SMH, Rajebi H, Moghaddas F, Ghasemiadl M, Talari H. Chest CT in COVID-19 pneumonia: what are the findings in mid-term follow-up? Emergency Radiology 2020:1–9.
- Zhao YM, Shang YM, Song WB, Li QQ, Xie H, Xu QF, Jia JL, Li LM, Mao HL, Zhou XM, Luo H, Gao YF, Xu AG. Follow-up study of the pulmonary function and related physiological characteristics of COVID-19 survivors three months after recovery. EClinicalMedicine 2020;25:100463. 10.1016/j.eclinm.2020.100463
- Hu Q, Guan H, Sun Z, Huang L, Chen C, Ai T, Pan Y, Xia L. Early CT features and temporal lung changes in COVID-19 pneumonia in Wuhan, China. Eur J Radiol 2020;128:109017. 10.1016/j.ejrad.2020.109017
- Huang G, Gong T, Wang G, Wang J, Guo X, Cai E, Li S, Li X, Yu Y, Lin L. Timely Diagnosis and Treatment Shortens the Time to Resolution of Coronavirus Disease (COVID-19) Pneumonia and Lowers the Highest and Last CT Scores From Sequential Chest CT. AJR Am J Roentgenol 2020;215(2):367–373. 10.2214/AJR.20.23078
- Liu N, He G, Yang X, Chen J, Wu J, Ma M, Lu W, Li Q, Cheng T, Huang X. Dynamic changes of Chest CT follow-up in Coronavirus Disease-19 (COVID-19) pneumonia: relationship to clinical typing. BMC Med Imaging 2020;20(1):92. 10.1186/s12880-020-00491-2
- Yu M, Liu Y, Xu D, Zhang R, Lan L, Xu H. Prediction of the Development of Pulmonary Fibrosis Using Serial Thin-Section CT and Clinical Features in Patients Discharged after Treatment for COVID-19 Pneumonia. Korean J Radiol 2020;21(6):746–755. 10.3348/kjr.2020.0215
- Ojha V, Mani A, Pandey NN, Sharma S, Kumar S. CT in coronavirus disease 2019 (COVID-19): a systematic review of chest CT findings in 4410 adult patients. Eur Radiol 2020;30(11):6129–6138. 10.1007/s00330-020-06975-7
- Salehi S, Abedi A, Balakrishnan S, Gholamrezanezhad A. Coronavirus Disease 2019 (COVID-19): A Systematic Review of Imaging Findings in 919 Patients. AJR Am J Roentgenol 2020;215(1):87–93. 10.2214/AJR.20.23034
- Han X, Fan Y, Alwalid O, Li N, Jia X, Yuan M, Li Y, Cao Y, Gu J, Wu H, Shi H. Six-Month Follow-up Chest CT findings after Severe COVID-19 Pneumonia. Radiology 2021:203153. 10.1148/radiol.2021203153
- Wells AU, Devaraj A, Desai SR. Interstitial Lung Disease after COVID-19 Infection: A Catalog of Uncertainties. Radiology 2021;299(1):E216–e218. 10.1148/radiol.2021204482
- Salehi S, Reddy S, Gholamrezanezhad A. Long-term Pulmonary Consequences of Coronavirus Disease 2019 (COVID-19): What We Know and What to Expect. J Thorac Imaging 2020;35(4):W87–W89. 10.1097/RTI.0000000000000534
- Zhang P, Li J, Liu H, Han N, Ju J, Kou Y, Chen L, Jiang M, Pan F, Zheng Y, Gao Z, Jiang B. Long-term bone and lung consequences associated with hospital-acquired severe acute respiratory syndrome: a 15-year follow-up from a prospective cohort study. Bone Res 2020;8:8. 10.1038/s41413-020-0084-5
- Wu X, Dong D, Ma D. Thin-Section Computed Tomography Manifestations During Convalescence and Long-Term Follow-Up of Patients with Severe Acute Respiratory Syndrome (SARS). Med Sci Monit 2016;22:2793–2799. 10.12659/msm.896985
- Clinical management of severe acute respiratory infection (SARI) when COVID-19 disease is suspected .
- Hansell DM, Goldin JG, King TE, Jr., Lynch DA, Richeldi L, Wells AU. CT staging and monitoring of fibrotic interstitial lung diseases in clinical practice and treatment trials: a position paper from the Fleischner Society. Lancet Respir Med 2015;3(6):483–496. 10.1016/S2213-2600(15)00096-X
- Hansell DM, Bankier AA, MacMahon H, McLoud TC, Muller NL, Remy J. Fleischner Society: glossary of terms for thoracic imaging. Radiology 2008;246(3):697–722. 10.1148/radiol.2462070712
- Yang R, Li X, Liu H, Zhen Y, Zhang X, Xiong Q, Luo Y, Gao C, Zeng W. Chest CT severity score: an imaging tool for assessing severe COVID-19. Radiology: Cardiothoracic Imaging 2020;2(2):e200047.
- Chen A, Karwoski RA, Gierada DS, Bartholmai BJ, Koo CW. Quantitative CT Analysis of Diffuse Lung Disease. Radiographics 2020;40(1):28–43. 10.1148/rg.2020190099
- Colombi D, Bodini FC, Petrini M, Maffi G, Morelli N, Milanese G, Silva M, Sverzellati N, Michieletti E. Well-aerated lung on admitting chest CT to predict adverse outcome in COVID-19 pneumonia. Radiology 2020:201433.
- Vernuccio F, Giambelluca D, Cannella R, Lombardo FP, Panzuto F, Midiri M, Cabassa P. Radiographic and chest CT imaging presentation and follow-up of COVID-19 pneumonia: a multicenter experience from an endemic area. Emerg Radiol 2020;27(6):623–632. 10.1007/s10140-020-01817-x
- Chen Y, Klein SL, Garibaldi BT, Li H, Wu C, Osevala NM, Li T, Margolick JB, Pawelec G, Leng SX. Aging in COVID-19: Vulnerability, immunity and intervention. Ageing Res Rev 2021;65:101205. 10.1016/j.arr.2020.101205
- Lyu P, Liu X, Zhang R, Shi L, Gao J. The Performance of Chest CT in Evaluating the Clinical Severity of COVID-19 Pneumonia: Identifying Critical Cases Based on CT Characteristics. Invest Radiol 2020;55(7):412–421. 10.1097/RLI.0000000000000689
- Lanza E, Muglia R, Bolengo I, Santonocito OG, Lisi C, Angelotti G, Morandini P, Savevski V, Politi LS, Balzarini L. Quantitative chest CT analysis in COVID-19 to predict the need for oxygenation support and intubation. Eur Radiol 2020;30(12):6770–6778. 10.1007/s00330-020-07013-2
- Gebhard C, Regitz-Zagrosek V, Neuhauser HK, Morgan R, Klein SL. Impact of sex and gender on COVID-19 outcomes in Europe. Biol Sex Differ 2020;11(1):29. 10.1186/s13293-020-00304-9
Source: PubMed