Multimodality imaging of COVID-19 pneumonia: from diagnosis to follow-up. A comprehensive review

Abstract

Due to its pandemic diffusion, SARS- CoV-2 (Severe Acute Respiratory Syndrome Coronavirus 2) infection represents a global threat. Despite a multiorgan involvement has been described, pneumonia is the most common manifestation of COVID-19 (Coronavirus disease 2019) and it is associated with a high morbidity and a considerable mortality. Especially in the areas with high disease burden, chest imaging plays a crucial role to speed up the diagnostic process and to aid the patient management. The purpose of this comprehensive review is to understand the diagnostic capabilities and limitations of chest X-ray (CXR) and high-resolution computed tomography (HRCT) in defining the common imaging features of COVID-19 pneumonia and correlating them with the underlying pathogenic mechanisms. The evolution of lung abnormalities over time, the uncommon findings, the possible complications, and the main differential diagnosis occurring in the pandemic phase of SARS-CoV-2 infection are also discussed.

Keywords: COVID-19 pneumonia; Chest X-ray; Diagnosis; Differential diagnosis; Follow-up; High-resolution computed tomography.

Fig. 1

Worsening evolution of COVID-19 pneumonia in a 63- year-old male with known cardiac disease (note the presence of a pacemaker). The first antero-posterior (AP) chest X-ray (CXR) (a) shows hazy opacities with a mid-basal and peripheral predominance on the right lung, without pleural effusion. Two days later, the AP CXR (b) depicts confluent and bilateral alveolar opacities with air bronchogram and quite diffuse distribution. CXR performed 9 days later in ICU (c) shows a further increase of bilateral alveolar opacities, especially in the mid-basal lungs. In the last CXR (d), a further radiographic worsening was evident, with development of bilateral "whited lung”. The patient deceased two days later due to ARDS.

Fig. 2

Common findings of COVID-19 pneumonia in two different patients. In the first patient, the axial HRCT image (a) shows bilateral, dorsal, subpleural areas of crazy paving. In the second patient, the axial HRCT image (b) demonstrates patchy bilateral consolidations with subpleural and dorsal distribution, and lower lobes volume loss. Chest X-ray (CXR) (c) of the same case as in b nicely depicts the bilateral peripheral mid-basal distribution of the opacities.

Fig. 3

Axial HRCT image (a) and maximum intensity projection (MIP) (b) in the early phase of COVID-19 pneumonia show enlargement (>3 mm) of a segmental pulmonary artery within the GG area in the apico- posterior segment of the left upper lobe (arrowhead in a and in b). Axial HRCT MIP image (c), performed 10 days later, shows a normal caliber of the same vessel at the same anatomical level (arrowhead in c). Note the consensual shrinkage of the focal GG area.

Fig. 4

Temporal evolution of COVID-19 pneumonia on HRCT. Axial (a) and coronal (b) HRCT images show bilateral GG opacities with a predominant peripheral distribution, located in the mid-upper lungs (early phase disease). Axial (c) and coronal (d) HRCT performed 9 days later demonstrate the typical evolution in the progressive phase, with extensive consolidations in the same areas previously involved by GG opacities. Note the overall mild lung volume reduction in d.

Fig. 5

Temporal evolution of COVID-19 pneumonia on chest X-ray (CXR) in the same patient as in Fig. 4. The first AP CXR (a) performed to admission in the emergency room shows ill-defined hazy opacities in the peripheral regions of both lung, especially in the left mid-zone and in the right lung base. Images (b) and (c), performed 4 and 7 days later, respectively, demonstrate a progressive increase of the opacities in terms of extension and density with progressive lung volume reduction in c. Patient experienced a clinical and radiological improvement two weeks later with reduction of lung opacities (d).

Fig. 6

Axial HRCT image (a) depicts traction bronchiectasis (arrowheads) within the peripheral area of consolidation in the left lower lobe, in a case of COVID-19 pneumonia in the progressive phase. The axial HRCT mIP (minimum intensity projection) image (b) enhances the visibility of traction bronchiectasis and bronchiolectasis within the same area (arrowhead).

Fig. 7

Progressive (a, c) and absorption stages (b, d) on HRCT of two different patients with COVID-19 pneumonia. In the first patient, the axial HRCT image in the progressive stage (a) demonstrates areas of consolidation with mild parenchymal retraction and traction bronchiectasis (arrowhead). The axial HRCT performed 12 days later (b) shows bilateral GG opacities which are more extended than the previously detected consolidation (“tinted” sign). Traction bronchiectasis within the GG opacities are still present (arrowheads). These findings should always be interpreted, looking at the previous scans, as normal evolution towards the resolution of abnormalities and not as persistent or worsening disease after a complete clinical recovery. In the second patient, the axial HRCT image in the progressive stage (c) depicts consolidations, mild GG opacities and perilobular opacities (arrow), more extensive in the right lung. The axial HRCT performed 16 days later (d) demonstrates almost complete resolution of the findings, with some residual faint ill-defined GG areas and linear opacities.

Fig. 8

Axial HRCT images (a, b) in two different patients with uncommon findings of COVID-19 pneumonia due to emphysema. In a, an uncommon unilateral GG and consolidation with subpleural sparing due to paraseptal emphysema is nicely depicted. In b, mixed GG and consolidation areas, containing apparent cystic-like changes due to centrilobular emphysema, are evident predominantly in the right lung. Axial (c) and coronal (d) HRCT images of a 77-year-old male with COVID-19 pneumonia showing bilateral subpleural and peribronchovascular consolidations with mild GG. A 3- cm, subpleural, pseudonodular, part-solid lesion with cystic-like airspaces, irregular margins, and pleural retraction is detected in the posterior segment of the right upper lobe (arrowheads); a lung adenocarcinoma was suspected on the basis of morphological features and confirmed at biopsy.

Fig. 9

Complications in two patients with severe COVID-19 pneumonia. In the first patient, axial HRCT image (a) demonstrates marked spontaneous pneumomediastinum and chest wall subcutaneous emphysema, associated with left pneumothorax. One week before, due to worsening dyspnoea, the patient had undergone CT scan with contrast medium injection to rule out pulmonary embolism (PE). Axial CT image (b) demonstrates a filling defect in the distal tract of the interlobar artery (arrowhead) due to acute PE. Note the shrinkage of the bilateral subpleural consolidations in the later CT scan (a). In the second patient, axial HRCT images (c, d) show focal consolidations with cavitation in the right upper lobe and some small consolidations in the left lung, superimposed on diffuse GG and septal thickening. A bacterial superinfection on COVID-19 pneumonia was suspected and the bronchoalveolar lavage confirmed a Pseudomonas aeruginosa infection.

Fig. 10

50-year-old male complaining of fever, chills and cough for 5 days. Chest X-ray (a) demonstrated a peripheral homogeneous opacity in the left upper lobe, suggestive of pneumonia with a sublobar nonsegmental appearance. Multiple RT-PCR tests resulted negative for SARS-CoV-2. Axial (b) and coronal (c) HRCT images confirm a peripheral sublobar nonsegmental consolidation with air bronchogram and mild adjacent GG in the left upper lobe. Microbiological tests were positive for Streptococcus pneumoniae.

Fig. 11

Axial HRCT images (a, b) in two different patients with a diagnosis of Mycoplasma pneumonia (a) and COVID-19 pneumonia (b), respectively. In a, patchy lobular and partially confluent consolidations and GG opacities, associated with centrilobular nodules and thickening of the peribronchovascular interstitium, are evident in the lower lobes. These findings allowed a confident differential diagnosis with COVID-19 pneumonia, shown in b, characterized by mixed GG and consolidations areas with a predominant peripheral/subpleural distribution in both lungs.

Fig. 12

72-year-old male complaining of fever and dry cough. Chest X-ray (a) shows multiple confluent nodules and opacities in the mid-upper right lung, findings unlikely related to COVID-19 pneumonia. Axial (b) and coronal (c) HRCT images confirm the presence of multiple confluent centrilobular GG nodules and lobular areas in the right upper lobe and in the apical segment of the right lower lobe, suggestive of a bronchopneumonia pattern of infection, not related to COVID-19 pneumonia. Test was negative for SARS-CoV-2, while a diagnosis of Metapneumovirus pneumonitis was made.

Fig. 13

83-year-old male with history of acute coronary syndrome, complaining of severe dyspnoea and cough. The AP chest X-ray (CXR) at admission shows interstitial- alveolar opacities, with peribronchovascular and mid- basal distribution, associated with peribronchial cuffing, vessel blurring, prominence of the proximal pulmonary vessels and mild bilateral pleural effusion (a). A cardiogenic pulmonary oedema was suspected. Swab tests for COVID-19 were negative while high level of NT-proBNP (N-terminal-pro-B-type natriuretic peptide) was detected. Echocardiography showed reduced ejection fraction (35 %). The CXR performed after 5 days of treatment with diuretics demonstrates complete resolution of the pulmonary findings (b).

Fig. 14

70-year-old male affected by connective tissue disease-interstitial lung disease (CTD-ILD), admitted to the emergency department with worsening dyspnoea over the last two weeks; the patient presented with diffuse bilateral velcro- like crackles. The HRCT scan was performed with contrast administration to rule out PE. Axial (a) and coronal (b) HRCT images show bilateral diffuse GG opacities, more evident within the left lung, in areas not extensively involved by fibrotic changes. Comparison with the HRCT exam performed one year earlier (c, d) demonstrates the new onset of diffuse GG opacities. COVID-19 swab resulted negative and a diagnosis of acute exacerbation of pulmonary fibrosis was made.

Fig. 15

HRCT images in two different patients with a diagnosis of aspiration pneumonia (a, b) and lipoid pneumonia (c, d), respectively. In the axial (a) and sagittal (b) images, a decumbent consolidation in the left lower lobe, associated with centrilobular micronodules and tree-in-bud opacities in the same lobe and in dorsal regions of the left upper lobe, is presented in a recumbent patient with recent tracheostomy. Note the left parapneumonic pleural effusion, which is an uncommon finding in COVID-19 pneumonia. In c, predominant peribronchovascular consolidations associated with mild crazy paving in the lower lobes and lingula, are shown in a patient with chronic use of vaseline. Note, in the mediastinal window image (d), the low attenuation values within consolidations, indicative of fat content (-40 HU). Distribution and attenuation of consolidations allowed an easy rule out of COVID-19 pneumonia.

Fig. 16

62-year-old female affected by granulomatosis with polyangiitis (GPA) and chronic renal failure (note the ultrafiltration catheter on the right) admitted to the emergency department because of progressive shortness of breath over the last few days. Haemoptysis was not reported. AP chest X-ray (CXR) (a) demonstrates bilateral ill-defined opacities (more diffuse on the right), with peribronchovascular distribution and sparing of subpleural regions, apices and bases. Coronal HRCT image (b) shows bilateral confluent consolidations with the same distribution, associated with GG opacities, ill-defined centrilobular nodules and few septal thickening. On the basis of clinical data and radiological pattern, a diagnosis of diffuse alveolar haemorrhage was made. RT-PCR essay resulted negative for SARS-CoV-2.