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Clinical, radiological and pathological findings in patients with persistent lung disease following SARS-CoV-2 infection

Claudia Ravaglia, Claudio Doglioni, Marco Chilosi, Sara Piciucchi, Alessandra Dubini, Giulio Rossi, Federica Pedica, Silvia Puglisi, Luca Donati, Sara Tomassetti, Venerino Poletti
European Respiratory Journal 2022 60: 2102411; DOI: 10.1183/13993003.02411-2021
Claudia Ravaglia
1Dept of Thoracic Diseases, G.B. Morgagni Hospital/University of Bologna, Forlì, Italy
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  • For correspondence: claudiaravaglia79@gmail.com
Claudio Doglioni
2Dept of Pathology, University Vita-Salute, Milan and San Raffaele Scientific Institute, Milan, Italy
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Marco Chilosi
3Dept of Pathology, Pederzoli Hospital, Peschiera del Garda, Italy
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Sara Piciucchi
4Dept of Radiology, G.B. Morgagni Hospital/University of Bologna, Forlì, Italy
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  • ORCID record for Sara Piciucchi
Alessandra Dubini
5Dept of Pathology, G.B. Morgagni Hospital/University of Bologna, Forlì, Italy
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Giulio Rossi
6Dept of Pathology, Fondazione Poliambulanza Istituto Ospedaliero Multispecialistico, Brescia, Italy
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Federica Pedica
7Dept of Pathology, San Raffaele Scientific Institute, Milan, Italy
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Silvia Puglisi
1Dept of Thoracic Diseases, G.B. Morgagni Hospital/University of Bologna, Forlì, Italy
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Luca Donati
8Biostatistics and Clinical Trial Unit, Istituto Romagnolo per lo Studio dei Tumori “Dino Amadori”-IRST S.r.l., IRCCS, Meldola, Italy
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Sara Tomassetti
9Dept of Experimental and Clinical Medicine, Careggi University Hospital, Firenze, Italy
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Venerino Poletti
1Dept of Thoracic Diseases, G.B. Morgagni Hospital/University of Bologna, Forlì, Italy
10DIMES, University of Bologna, Bologna, Italy
11Dept of Respiratory Diseases and Allergy, Aarhus University Hospital, Aarhus, Denmark
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  • FIGURE 1
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    FIGURE 1

    Computed tomography (CT) scan in a 60-year-old male smoker. a–c) During acute infection, mild peripheral ground-glass attenuation is present in both upper lobes, mainly in the left hemithorax (red circle). Scattered areas of cystic changes suggestive of airspace enlargement with associated fibrosis (AEF) with mild architectural distortion are present bilaterally. d–f) A CT scan performed 4 months later shows a reduction in ground-glass attenuation, with residual ground-glass attenuation and areas of AEF (f, green arrow).

  • FIGURE 2
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    FIGURE 2

    Computed tomography (CT) scan in a 62-year-old man with a–c) acute COVID infection characterised by bilateral, peripheral consolidations (b, blue arrow) and perilobular pattern (c, red arrow). d–f) A CT scan performed 2 months later shows mild peripheral reticulation and minimal perilobular pattern, mainly in the right lower lobe (f, yellow circle).

  • FIGURE 3
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    FIGURE 3

    Computed tomography (CT) scan in a 50-year-old man with a–c) COVID-related acute pneumonia with extensive, peribronchovascular consolidations in both lungs and lobular sparing in both lower lobes. Moderate ground-glass attenuation is present in both upper lobes associated with vessel enlargement (c, blue circle). d–f) A CT scan performed 2 months later shows mild, diffuse ground-glass attenuation in both lungs associated with central bronchiectasis in the middle lobe and in both lower lobes.

  • FIGURE 4
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    FIGURE 4

    a) Cluster 1. A case with a usual interstitial pneumonia pattern: architectural distortion, spatial and temporal heterogeneity of scarring modifications and microscopic honeycombing. Haematoxylin and eosin (H&E) staining ×10 magnification. b) Cluster 2. A case with morphological evidence of ongoing interstitial fibrosis and extended alveolar epithelial type II cell hyperplasia as observed in diffuse alveolar damage, proliferative phase. H&E staining. c) Cluster 2. Cytokeratin 7 immunostaining of epithelial cells, at low magnification, showing the severe effacement of parenchymal structure. d) A case with organising pneumonia pattern. H&E staining. e) Most epithelial cells and endothelial cells express nuclear phosphorylated signal transducer and activator of transcription 3. b–e ×20 magnification.

  • FIGURE 5
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    FIGURE 5

    Cluster 3. A case with diffuse vascular increase, dilatation and distortion (both capillaries and venules) within an otherwise normal parenchyma. a) Haematoxylin and eosin staining ×10 magnification, b) cytokeratin 7 immunostaining, c) diffuse and strong endothelial expression of phosphorylated signal transducer and activator of transcription 3, d) indoleamine 2, 3-dioxygenase and e) programmed cell death 1 ligand 1. b–e ×20 magnification.

Tables

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  • TABLE 1

    Radiological and pathological findings in patients with persistent lung disease

    Acute phase HRCTPost-acute phase HRCTTime from recovery (days)Histology
    Patient 1Peripheral consolidation, mild crazy paving (OP-like pattern)Reticulation with some perilobular pattern, traction bronchiectasis100AECII hyperplasia, honeycombing, patchy fibrosis, fibroblastic foci, lymphoid nodules
    Patient 2Bilateral ground glass, vessel enlargement (venoplegic hyperhemic pattern), smoking-related ILD (AEF+emphysema)Mild peripheral ground glass, smoking-related ILD (AEF+emphysema)227AECII hyperplasia, interstitial fibrosis, perivascular fibrosis, lymphoid nodules, macrophages containing light brown pigment
    Patient 3Not performedPeripheral consolidation, ground glass, vessel enlargement (gravity-dependent perilobular pattern)32AECII hyperplasia, OP, vascular dilatation, perivascular fibrosis, perivascular lymphocytes, lymphoid nodules
    Patient 4Peripheral consolidation, ground glass, vessel enlargement (gravity-dependent perilobular pattern)Scattered bronchial ectasis, no fibrotic distortion, mild perilobular pattern65OP
    Patient 5Ground glass, vessel enlargement, (venoplegic/hyperhaemic pattern in a background of ILA)Stable ILA, mild ground-glass attenuation with mild perilobular pattern76AECII hyperplasia, perivascular lymphocytes, interstitial fibrosis
    Patient 6Ground glass, vessel enlargement (venoplegic/hyperhaemic pattern)Extensive consolidations, halo sign, reverse halo sign, perilobular pattern160AECII hyperplasia, OP, vascular dilatation, perivascular fibrosis, perivascular lymphocytes, interstitial fibrosis
    Patient 7Not performedGround glass, vessel enlargement (venoplegic/hyperaemic pattern in a background of NSIP-OP)56AECII hyperplasia, perivascular lymphocytes, interstitial fibrosis
    Patient 8Peripheral consolidation, ground glass, vessel enlargement (gravity-dependent perilobular pattern)Mild residual ground glass with perilobular pattern123Vascular dilatation, perivascular fibrosis
    Patient 9Ground glass, vessel enlargement (venoplegic/hyperhaemic pattern)Mild residual ground glass with perilobular pattern137Minimal patchy AECII, vascular dilatation, perivascular fibrosis
    Patient 10Not performedPPFE, mild ground glass44Vascular dilatation, perivascular fibrosis

    HRCT: high-resolution computed tomography; OP: organising pneumonia; AECII: alveolar epithelial type 2 cells; ILD: interstitial lung disease; AEF: airspace enlargement with fibrosis; ILA: interstitial lung abnormalities; NSIP: nonspecific interstitial pneumonia; PPFE: pleuro-parenchymal fibroelastosis.

    • TABLE 2

      Identification of possible subgroups (clusters) of patients with post-acute COVID-19

      Clinical pictureRadiological patternHistopathology
      Cluster 1Respiratory symptoms (cough, dyspnoea), no systemic symptoms, compromised DLCOInterstitial lung disease, lung fibrotic appearances with architectural distortion, traction bronchiectasisUIP or fibrosing interstitial pneumonia, spatial and temporal heterogeneity of scarring modifications, fibroblast foci, honeycombing
      Cluster 2Respiratory symptoms (cough, dyspnoea), systemic symptoms (fever, fatigue), compromised DLCOPeripheral consolidation, ground glass, perilobular pattern, vessel enlargement, reverse halo signLung injury, OP, OP/NSIP, diffuse alveolar damage, no hyaline membranes, lymphocytic inflammatory infiltrate
      Cluster 3Respiratory symptoms (cough, dyspnoea), systemic symptoms (fatigue, aches), normal DLCOMild residual lung disease, mild ground glass, perilobular patternDiffuse vascular increase, dilatation and distortion (capillaries and venules), otherwise normal parenchyma

      DLCO: diffusing capacity of the lung for carbon monoxide; UIP: usual interstitial pneumonia; OP: organising pneumonia; NSIP: nonspecific interstitial pneumonia.

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        Supplementary material ERJ-02411-2021.SUPPLEMENT

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        Shareable PDF ERJ-02411-2021.Shareable

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      Clinical, radiological and pathological findings in patients with persistent lung disease following SARS-CoV-2 infection
      Claudia Ravaglia, Claudio Doglioni, Marco Chilosi, Sara Piciucchi, Alessandra Dubini, Giulio Rossi, Federica Pedica, Silvia Puglisi, Luca Donati, Sara Tomassetti, Venerino Poletti
      European Respiratory Journal Oct 2022, 60 (4) 2102411; DOI: 10.1183/13993003.02411-2021

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      Clinical, radiological and pathological findings in patients with persistent lung disease following SARS-CoV-2 infection
      Claudia Ravaglia, Claudio Doglioni, Marco Chilosi, Sara Piciucchi, Alessandra Dubini, Giulio Rossi, Federica Pedica, Silvia Puglisi, Luca Donati, Sara Tomassetti, Venerino Poletti
      European Respiratory Journal Oct 2022, 60 (4) 2102411; DOI: 10.1183/13993003.02411-2021
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