Pulmonary circulation abnormalities in post-acute COVID-19 syndrome: dual-energy CT angiographic findings in 79 patients.


Journal

European radiology
ISSN: 1432-1084
Titre abrégé: Eur Radiol
Pays: Germany
ID NLM: 9114774

Informations de publication

Date de publication:
Jul 2023
Historique:
received: 08 12 2022
accepted: 06 03 2023
revised: 26 02 2023
medline: 26 6 2023
pubmed: 5 5 2023
entrez: 5 5 2023
Statut: ppublish

Résumé

To evaluate the frequency and pattern of pulmonary vascular abnormalities in the year following COVID-19. The study population included 79 patients remaining symptomatic more than 6 months after hospitalization for SARS-CoV-2 pneumonia who had been evaluated with dual-energy CT angiography. Morphologic images showed CT features of (a) acute (2/79; 2.5%) and focal chronic (4/79; 5%) PE; and (b) residual post COVID-19 lung infiltration (67/79; 85%). Lung perfusion was abnormal in 69 patients (87.4%). Perfusion abnormalities included (a) perfusion defects of 3 types: patchy defects (n = 60; 76%); areas of non-systematized hypoperfusion (n = 27; 34.2%); and/or PE-type defects (n = 14; 17.7%) seen with (2/14) and without (12/14) endoluminal filling defects; and (b) areas of increased perfusion in 59 patients (74.9%), superimposed on ground-glass opacities (58/59) and vascular tree-in-bud (5/59). PFTs were available in 10 patients with normal perfusion and in 55 patients with abnormal perfusion. The mean values of functional variables did not differ between the two subgroups with a trend toward lower DLCO in patients with abnormal perfusion (74.8 ± 16.7% vs 85.0 ± 8.1). Delayed follow-up showed CT features of acute and chronic PE but also two types of perfusion abnormalities suggestive of persistent hypercoagulability as well as unresolved/sequelae of microangiopathy. Despite dramatic resolution of lung abnormalities seen during the acute phase of the disease, acute pulmonary embolism and alterations at the level of lung microcirculation can be identified in patients remaining symptomatic in the year following COVID-19. • This study demonstrates newly developed proximal acute PE/thrombosis in the year following SARS-CoV-2 pneumonia. • Dual-energy CT lung perfusion identified perfusion defects and areas of increased iodine uptake abnormalities, suggestive of unresolved damage to lung microcirculation. • This study suggests a complementarity between HRCT and spectral imaging for proper understanding of post COVID-19 lung sequelae.

Identifiants

pubmed: 37145145
doi: 10.1007/s00330-023-09618-9
pii: 10.1007/s00330-023-09618-9
pmc: PMC10129318
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4700-4712

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2023. The Author(s), under exclusive licence to European Society of Radiology.

Références

Nalbandian A, Sehgal K, Gupta A et al (2021) Post-acute COVID-19 syndrome. Nat Med 27:601–615
doi: 10.1038/s41591-021-01283-z pubmed: 33753937 pmcid: 8893149
(2020) COVID-19 rapid guideline: managing the long-term effects of COVID-19. London, National Institute for Health and Care Excellence (UK). Available from  www.ncbi.nih.gov/books/NBK567261/ . Accessed June 2022
Groff D, Sun A, Ssentongo AE et al (2021) Short-term and long-term rates of postacute sequelae of SARS-CoV-2 infection: a systematic review. JAMA Netw Open 4:e2128568
doi: 10.1001/jamanetworkopen.2021.28568 pubmed: 34643720 pmcid: 8515212
Huang L, Yao Q, Gu X et al (2021) 1-year outcomes in hospital survivors with COVID-19: a longitudinal cohort study. Lancet 398:747–758
doi: 10.1016/S0140-6736(21)01755-4 pubmed: 34454673 pmcid: 8389999
Darcis G, Bouquegneau A, Maes N et al (2021) Long-term clinical follow-up of patients suffering from moderate-to-severe COVID-19 infection: a monocentric prospective observational cohort study. Int J Infect Dis 109:209–216
doi: 10.1016/j.ijid.2021.07.016 pubmed: 34273510 pmcid: 8278829
George PM, Desai SR (2021) COVID-19 pneumonia and the pulmonary vasculature: a marriage in hell. Eur Respir J 58:2100811
doi: 10.1183/13993003.00811-2021 pubmed: 33863736 pmcid: 8051183
Oudkerk M, Kuijpers D, Oudkerk SF, Van Beek EJR (2020) The vascular nature of COVID-19. Br J Radiol 93:20200718
doi: 10.1259/bjr.20200718 pubmed: 32735457 pmcid: 7465848
McGonagle D, Bridgewood C, Ramanan AV et al (2021) COVID-19 vasculitis and novel vasculitis mimics. Lancet Rheumatol 3:e224–e233
doi: 10.1016/S2665-9913(20)30420-3 pubmed: 33521655 pmcid: 7832717
Ackerman M, Verleden SE, Kuehnel M et al (2020) Pulmonary vascular endothelialitis, thrombosis and angiogenesis in COVID-19. N Engl J Med 383:120–128
doi: 10.1056/NEJMoa2015432
Varga Z, Flammer AJ, Steiger P et al (2020) Endothelial cell infection and endotheliitis in COVID-19. Lancet 395(10234):1417–1418
doi: 10.1016/S0140-6736(20)30937-5 pubmed: 32325026 pmcid: 7172722
Fox SE, Akmatbekov A, Harbert JL et al (2020) Pulmonary and cardiac pathology in African American patients with COVID-19: an autopsy series from New Orleans. Lancet Respir Med 8:681–686
doi: 10.1016/S2213-2600(20)30243-5 pubmed: 32473124 pmcid: 7255143
Jimenez D, Garcia-Sanchez A, Rali P et al (2021) Incidence of VTE and bleeding among hospitalized patients with coronavirus disease in 2019. Chest 159:1182–1196
doi: 10.1016/j.chest.2020.11.005 pubmed: 33217420
Suh YJ, Hong H, Ohana M et al (2021) Pulmonary embolism and deep vein thrombosis in COVID-19: a systematic review and meta-analysis. Radiology 298: E70-E80
Tan BK, Mainbourg S, Friggeri A et al (2021) Arterial and venous thromboembolism in COVID-19: a study-level meta-analysis. Thorax 76:970–979
doi: 10.1136/thoraxjnl-2020-215383 pubmed: 33622981
Goddard S, Tran DQ, Chan MF et al (2021) Pulmonary vein thrombosis in COVID-19. Chest 159:e361–e364
doi: 10.1016/j.chest.2020.11.064 pubmed: 34099150
Patel BV, Arachchillage DJ, Ridge CA et al (2020) Pulmonary angiopathy in severe COVID-19: physiologic, imaging and hematologic observations. Am J Respir Crit Care Med 202:690–699
doi: 10.1164/rccm.202004-1412OC pubmed: 32667207 pmcid: 7462405
Santamarina MG, Riscal DB, Beddings I et al (2020) COVID-19: what iodine maps from perfusion CT can reveal – a prospective cohort study. Crit Care 24:619
doi: 10.1186/s13054-020-03333-3 pubmed: 33087155 pmcid: 7576979
Idilman IS, Dizman GT, Duzgun SA et al (2021) Lung and kidney perfusion deficits diagnosed with dual-energy computed-tomography in patients with COVID-19-related systemic microangiopathy. Eur Radiol 31:1090–1099
doi: 10.1007/s00330-020-07155-3 pubmed: 32860146
Grillet F, Busse-Coté A, Calame P et al (2020) COVID-19 pneumonia: microvascular disease revealed on pulmonary dual-energy computed tomography angiography. Quant Imaging Med Surg 10:1852–1862
doi: 10.21037/qims-20-708 pubmed: 32879862 pmcid: 7417764
Aydin S, Kantarci M, Karavas E et al (2021) Lung perfusion changes in COVID-19 pneumonia: a dual energy computerized tomography study. Br J Radiol 94:20201380
doi: 10.1259/bjr.20201380 pubmed: 34415201 pmcid: 9327758
Le Berre A, Boeken T, Caramella C et al (2021) Dual-energy CT angiography reveals high prevalence of perfusion defects unrelated to pulmonary embolism in COVID-19 lesions. Insights Imaging 12:2432
doi: 10.1186/s13244-021-00972-0
Patelli G, Paganoni S, Besena F et al (2020) Preliminary detection of lung hypoperfusion in discharged COVID-19 patients during recovery. Eur Respir J 129:109121
Remy-Jardin M, Duthoit L, Perez T et al (2021) Assessment of pulmonary arterial circulation 3 months after hospitalization for SARS-CoV-2 pneumonia: dual-energy CT (DECT) angiographic study in 55 patients. EClinicalMedicine 34:100778
doi: 10.1016/j.eclinm.2021.100778 pubmed: 33817609 pmcid: 8008988
Gierarts C, Dangis A, Janssen L et al (2022) Prognostic value and reproducibility of AI-assisted analysis of lung involvement in COVID-19 on low-dose submillisievert chest CT: sample size implications for clinical trials. Radiol Cardiothorac Imaging 2:e200441
doi: 10.1148/ryct.2020200441
Wanger J, Clausen JL, Coates A et al (2005) Standardisation of the measurement of lung volumes. Eur Respir J 26(3):511–522
doi: 10.1183/09031936.05.00035005 pubmed: 16135736
Miller MR, Hankinson J, Brusasco V et al (2005) Standardisation of spirometry. Eur Respir J 26(2):319 38
Macintyre N, Crapo RO, Viegi G et al (2005) Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J 26:720–735
doi: 10.1183/09031936.05.00034905 pubmed: 16204605
Pellegrino R, Viegi G, Brusasco V et al (2005) Interpretative strategies for lung function tests. Eur Respir J 26:948–968
doi: 10.1183/09031936.05.00035205 pubmed: 16264058
Overton PM, Toshner M, Mulligan C et al (2022). Pulmonary thromboembolic events in COVID-19 – a systematic literature review. Pulm Circ 5:e12113. https://doi.org/10.1002/pul2.12113
Rashidi F, Barco S, Kamangar F et al (2021) Incidence of symptomatic venous thromboembolism following hospitalization for coronavirus disease 2019: prospective results from a multi-center study. Thromb Res 198:135–138
doi: 10.1016/j.thromres.2020.12.001 pubmed: 33338976
Katsoularis I, Fonseca-Rodriguez O, Farrington P et al (2022) Risks of deep vein thrombosis, pulmonary embolism, and bleeding after COVID-19: nationwide self-controlled case series and matched cohort study. BMJ 2022(377):e069590
doi: 10.1136/bmj-2021-069590
Cueto-Robledo G, Roldan-Valadez E, Graniel-Palafox LE et al (2022) Chronic thrombo-embolic pulmonary hypertension (CTEPH): a review of another sequel of severe post-COVID-19 pneumonia. Curr Probl Cardiol 101187. https://doi.org/10.1016/j.cpcardiol.2022.101187
Ackermann M, Tafforeau P, Wagner WL et al (2022) The bronchial circulation in COVID-19 pneumonia. Am J Respir Crit Care Med 205:121–125
doi: 10.1164/rccm.202103-0594IM pubmed: 34734553
Galambos C, Bush D, Abman SH (2021) Intrapulmonary bronchopulmonary anastomoses in COVID-19 respiratory failure. Eur Respir J 58:2004397
doi: 10.1183/13993003.04397-2020 pubmed: 33863743 pmcid: 8051184
Ravaglia C, Doglioni C, Chilosi M et al (2022) Clinical, radiological and pathological findings in patients with persistent lung disease following SARS-CoV-2 infection. Eur Respir J 2102411. https://doi.org/10.1183/13993003.02411-2021
Mo X, Jian W, Su Z et al (2020) Abnormal pulmonary function in COVID-19 patients at the time of hospital discharge. Eur Respir J 55:2001217
doi: 10.1183/13993003.01217-2020 pubmed: 32381497 pmcid: 7236826
Frija-Masson J, Bancal C, Plantier L et al (2021) Alteration of diffusion capacity after SARS-CoV-2 infection: a pathophysiological approach. Front Physiol 12:624062
doi: 10.3389/fphys.2021.624062 pubmed: 33841169 pmcid: 8030254
Fortini A, Torrigiani A, Sbaragli S et al (2021) COVID-19: Persistence of symptoms and lung alterations after 3–6 months from hospital discharge. Infection 49:1007–1015
doi: 10.1007/s15010-021-01638-1 pubmed: 34091869 pmcid: 8179958
Zhao YM, Shang YM, Song WB et al (2020) Follow-up study of the pulmonary function and related physiological characteristics of COVID-19 survivors three months after recovery. EClinicalMedicine 25:100463
doi: 10.1016/j.eclinm.2020.100463 pubmed: 32838236 pmcid: 7361108
Balbi M, Conti C, Imeri G et al (2021) Post-discharge chest CT findings and pulmonary function tests in severe COVID-19 patients. Eur J Radiol 138:109676
doi: 10.1016/j.ejrad.2021.109676 pubmed: 33798931 pmcid: 7980523
Wu Q, Zhong L, Li H et al (2021) A follow-up study of lung function and chest computed tomography at 6 months after discharge in patients with coronavirus disease in 2019. Can Respir J 2021:6692409. https://doi.org/10.1155/2021/6692409 . eCollection 2021

Auteurs

Islam Mohamed (I)

Department of Thoracic Imaging, ULR 2694 METRICS Evaluation des technologies de Santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France.

Virginie de Broucker (V)

Department of Pulmonary Function Testing, ULR 4483, IMPECS, Univ. Lille, CHU Lille, F-59000, Lille, France.

Alain Duhamel (A)

Department of Biostatistics, ULR 2694 METRICS Evaluation des technologies de santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France.

Jessica Giordano (J)

Department of Thoracic Imaging, ULR 2694 METRICS Evaluation des technologies de Santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France.

Alice Ego (A)

Department of Thoracic Imaging, ULR 2694 METRICS Evaluation des technologies de Santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France.

Nicolas Fonne (N)

Department of Thoracic Imaging, ULR 2694 METRICS Evaluation des technologies de Santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France.

Cécile Chenivesse (C)

Department of Pulmonology, CNRS, INSERM, Institut Pasteur de Lille, U1019, UMR 9017, Center for Infection and Immunity of Lille (CIIL), Univ. Lille, CHU Lille, F-59000, Lille, France.

Jacques Remy (J)

Department of Thoracic Imaging, ULR 2694 METRICS Evaluation des technologies de Santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France.

Martine Remy-Jardin (M)

Department of Thoracic Imaging, ULR 2694 METRICS Evaluation des technologies de Santé et des pratiques médicales, Univ. Lille, CHU Lille, F-59000, Lille, France. martine.remy@chu-lille.fr.
Department of Thoracic Imaging, Heart & Lung Institute, University Hospital Center of Lille, Blvd Jules Leclercq, F-59000, Lille, France. martine.remy@chu-lille.fr.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH