key: cord-0767820-c5y8zft2
authors: Hochhegger, Bruno; Mandelli, Nicole S; Stüker, Guilherme; Meirelles, Gustavo Souza Portes; Zanon, Matheus; Mohammed, Tan-Lucien; Verma, Nupur; Sverzellati, Nicola; Marchiori, Edson
title: Coronavirus disease 2019 (COVID-19) pneumonia presentations in chest computed tomography: a pictorial review
date: 2020-06-27
journal: Curr Probl Diagn Radiol
DOI: 10.1067/j.cpradiol.2020.06.010
sha: 23a5c344789e80a33e5363eb2f8da6a6a71f81ce
doc_id: 767820
cord_uid: c5y8zft2

Despite imaging not being a tool for novel coronavirus disease 2019 (COVID-19) diagnosis, there has been an increased number of chest computed tomography (CT) scans done worldwide. There are no pathognomonic CT features for COVID-19 pneumonia, as findings are also common in other infectious diseases and noninfectious aetiologies. Nonetheless, point-of-care physicians should be familiarized with the most common imaging presentations of the COVID-19. In this pictorial review, we have summarized the most reported imaging features of COVID-19 pneumonia, including possible differential diagnosis according to the CT finding.

The novel coronavirus disease 2019 (COVID-19) is an RNA virus-based disease, which emerged in December of 2019 in Wuhan (China) and quickly spread worldwide. Due to its high infectivity, the World Health Organization (WHO) declared it a pandemic on March 11, 2020. 1 By April 1, 2020, there were nearly 800,000 confirmed cases in 205 countries and territories around the world and more than 37,000 deaths, according to the WHO reports. 1 The mean mortality rate is approximately 3% in the general population but could be higher in elderly patients with chronic comorbidities, such as diabetes, hypertension, and respiratory diseases. 2 In patients requiring mechanical ventilation, mortality could be up to 81%. 1, 2 In most COVID-19 cases, patients are asymptomatic. However, the most commonly reported symptoms are mild, ranging from fever (83-98%), cough (76-82%), and minimal respiratory distress to shortness of breath (31-55%), oxygen saturation <93%, and acute respiratory distress syndrome requiring mechanic ventilation. [1] [2] [3] So far, the gold-standard test for COVID-19 diagnosis is real-time reversetranscription-polymerase-chain-reaction (RRT-PCR). However, RRT-PCR is not readily available and demonstrates moderate to high rates of false-negative results. 1-3 Despite imaging not being a tool for COVID-19 diagnosis, there has been an increased number of chest computed tomography (CT) scans done worldwide to assess the severity and extension of lower respiratory tract involvement. 4 Plain chest radiography is often inaccurate in initial stages of the infection, while high-resolution CT is extremely sensitive for diagnosing ground-glass opacities (GGO). 5 However, there is still no consensus on the use of chest x-ray or CT for the management of suspected COVID-19 pneumonia, and the choice of imaging modality will depend on the physicians' judgment and local resources and expertise.

Nonetheless, point-of-care physicians should be familiarized with the most common imaging presentations of the COVID-19. In this pictorial review, we have summarized the most reported imaging features of COVID-19 pneumonia, including possible differential diagnosis according to the CT finding.

COVID-19 pneumonia presentation on imaging varies across the distinct stages of the disease, usually corresponding to different phases of organizing pneumonia or diffuse alveolar damage. 5.6 Some authors have proposed the following classification of COVID stages according to the interval between the onset of symptoms and the CT scan: early phase, 0 to 5 days; intermediate phase, 6 to 11 days; and late phase, 12 to 17 days. 6 In the early phase, the disease is mainly characterized by single or few rounded low-density GGO with a subpleural location. 6 However, it is worth emphasizing that 11-15% (sporadically up to approximately 50%) of patients may have normal CT scans 0-2 days after onset of flu-like symptoms from COVID-19. 6 In the intermediate phase, rounded GGO is commonly observed and may present more significant extension and density and a higher number of lesions. 6 At the late phase, the CT may present bilateral and diffuse areas of "white lung," secondary to large and confluent high-density GGOs, consolidations, air bronchograms, and interlobular/intralobular thickening. 6 The "crazy paving" pattern has been described to present, especially around day 10. 2 Also, during this stage, CT may demonstrate the "halo sign" and "reversed halo sign." At the final phase, lesions gradually reduce, and only some inter or intralobular septal thickening might be found. 6 Septal thickening as predominant finding appears after day 18 (Table 1) . 7 Pleural effusions and lymphadenopathy are rare findings. Furthermore, some reports have also described pulmonary thromboembolism as a CT pulmonary angiography finding in patients with COVID-19 ( Figure 1 ). 8 These CT findings are non-specific for COVID-19, as they may represent a significant number of differential diagnoses, both acute and chronic, such as other viral pneumonia, atypical bacterial pneumonia, inflammatory interstitial diseases, and organizing pneumonia. 1 Besides, some series have shown a 20% rate of other concomitant infections in PCR confirmed COVID-19 patients, which could further complicate the interpretation of the CT findings. 4 Therefore, it is crucial to have a high index of clinical suspicion and pre-test probability before interpreting the images. Based on references from other main articles, a summary of the key CT findings suggestive of COVID-19 pneumonia is presented in Table 2 .

GGOs are hazy opacities with increased lung attenuation and preservation of bronchial and vascular margins and include a vast number of differential diagnoses. 9 GGOs are the most common finding in COVID-19 patients, presenting as rounded opacities that can be seen since the early phase, most with bilateral involvement (Figures 2-4) . However, unilateral involvement could also be seen ( Figure 5 ). The distribution is often peripheral and subpleural but can also be along with the bronchovascular bundle. With disease progression, extensive areas of GGO can appear, commonly associated with consolidative opacities and sometimes presenting a "crazy paving" pattern.

Crazy-paving attenuation pattern is the superimposition of interlobular and intralobular septal thickening on a background of GGOs. 9 It represents pulmonary interstitial expansion, mostly caused by inflammation. 9 In COVID-19, this pattern is best seen in advanced disease, as the intermediate and later phases, which indicates increased involvement of the lung parenchyma. 6 ( Figure 6 ). "Crazy-paving" pattern is a characteristic finding of pulmonary alveolar proteinosis, lipoid pneumonia, non-specific interstitial pneumonia, and a limited number of other differential diagnoses.

Consolidations are homogeneous areas of increased lung attenuation that obscures the margins of vessels and airway walls. 9 In COVID-19 pneumonia, the intermediate and later

phases of the disease can present a CT pattern of the predominance of consolidation. This finding is associated with an inflammatory progression and is frequently seen with other concomitant areas of GGOs (Figures 7-8) . 4 These areas are represented by a cellular effusion which fills alveoli and causes vasodilatation with local exudation. 6 There is an extensive differential diagnosis for a consolidation pattern that could vary according to an acute or a chronic condition. [5] [6] [7] [8] 

The halo sign is a GGO surrounding a nodule or mass. 9 It often indicates a circumjacent area of haemorrhage around a lesion and might be seen in some patients with COVID-19 (Figure 9 ). 10 The halo sign is mostly seen in invasive pulmonary aspergillosis as well as other fungal infections such as Mucormycosis and Cryptococcosis. Neoplastic diseases such as pulmonary adenocarcinoma and some types of pulmonary metastasis can also present with this sign. Other differential diagnoses include tuberculosis, granulomatosis with polyangiitis, and eosinophilic lung diseases. 9 , 10

The reversed halo sign is represented by a GGO with a circumjacent ring of consolidation. 9 It was first described in cryptogenic organizing pneumonia and thought to be specific for this condition. 11 Later, chest CT showed this finding to be associated with other diseases like fungal infections (angioinvasive aspergillosis, paracoccidioidomycosis), tuberculosis, and other atypical and even typical bacterial infections, often in resolution phases. Further, the reversed halo sign, when seen in subpleural areas, remits to pulmonary infarction due to thromboembolism. Other differential diagnoses are vasculitis, inflammatory interstitial diseases, neoplasms, and actinic damage. 11

In COVID-19, the reversed halo sign is a less common feature and, when present, is identified in the later phases of the disease (Figures 10-11) . In one study with 121 patients with CT scans obtained in different COVID-19 stages, only 4% of patients in the late phase presented the reversed halo sign. In contrast, none of the patients in an early (0 to 2 days) or an intermediate (3 to 5 days) phases had this finding. 4

The "tree-in-bud" pattern is characterized by well or ill-defined centrilobular branching nodules that correspond to impaction within bronchioles and alveoli by fluid, mucus, or pus. 9 Presence of this finding in COVID-19 pneumonia is uncommon. 5 It could represent a concomitant condition, such as other infections (bronchopneumonia, fungal and mycobacterium infection), cystic fibrosis, chronic aspiration, autoimmune diseases, and some malignancies. 9, 11 Cavities are destructive lesions in the lung parenchyma characterized by air space within a consolidation, a nodule, or a mass, with variable wall thickness and can be filled by fluid. 9 Cavities may represent infections but also malignancies, autoimmune disorders, or pulmonary emboli. 9 So far, there are no reports of cavitary lesions in COVID-19 pneumonia, and its presence could indicate other associated diseases. 12 Mucoid impactions, bronchial wall thickening, lymphadenopathy, and pleural effusion, when isolated, are also not usual features in COVID-19 infection and leads to another diagnosis. 12

There are no pathognomonic CT findings for COVID-19 pneumonia, as they can also be seen with numerous pathogens and in many noninfectious aetiologies. CT scans should not be used as a diagnosis or screening tool for COVID-19 in asymptomatic patients.

GGO with diffuse distribution in both lungs. 7c and 7d coronal and sagittal CT reconstructions demonstrated the same findings in lower lobes. 

Coronavirus Disease 2019 (COVID-19): A Perspective from China

Clinical course and mortality risk of severe COVID-19. The Lancet

Differential diagnoses of illness in patients under investigation for the novel coronavirus

Chest CT Findings in Coronavirus Disease-19 (COVID-19): Relationship to Duration of Infection

Imaging Features of Coronavirus disease 2019 (COVID-19): Evaluation on Thin-Section CT. Academic Radiology

Coronavirus Disease (COVID-19): Spectrum of CT Findings and Temporal Progression of the Disease

Temporal Chances of CT Findings in 90 Patients with COVID-19 Pneumonia: A Longitudinal Study

Findings of Acute Pulmonary Embolism in COVID-19 Patients. The Lancet Infectious Diseases

Fleischner Society: Glossary of terms for thoracic imaging