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The Role of Chest Imaging in Patient Management During the COVID-19 Pandemic

With more than 900,000 confirmed cases worldwide and nearly 50,000 deaths during the first 3 months of 2020, the coronavirus disease 2019 (COVID-19) pandemic has emerged as an unprecedented health care crisis. The spread of COVID-19 has been heterogeneous, resulting in some regions having sporadic transmission and relatively few hospitalized patients with COVID-19 and others having community transmission that has led to overwhelming numbers of severe cases. For these regions, health care delivery has been disrupted and compromised by critical resource constraints in diagnostic testing, hospital beds, ventilators, and health care workers who have fallen ill to the virus exacerbated by shortages of personal protective equipment. Although mild cases mimic common upper respiratory viral infections, respiratory dysfunction becomes the principal source of morbidity and mortality as the disease advances. Thoracic imaging with chest radiography and CT are key tools for pulmonary disease diagnosis and management, but their role in the management of COVID-19 has not been considered within the multivariable context of the severity of respiratory disease, pretest probability, risk factors for disease progression, and critical resource constraints. To address this deficit, a multidisciplinary panel comprised principally of radiologists and pulmonologists from 10 countries with experience managing patients with COVID-19 across a spectrum of health care environments evaluated the utility of imaging within three scenarios representing varying risk factors, community conditions, and resource constraints. Fourteen key questions, corresponding to 11 decision points within the three scenarios and three additional clinical situations, were rated by the panel based on the anticipated value of the information that thoracic imaging would be expected to provide. The results were aggregated, resulting in five main and three additional recommendations intended to guide medical practitioners in the use of chest radiography and CT in the management of COVID-19.

. For example, CT screening of 82 asymptomatic individuals with confirmed COVID-19 from the cruise ship "Diamond Princess" showed findings of pneumonia in 54% (11).

Imaging Logistics During Pandemic
Provision of diagnostic imaging services to large numbers of patients suspected or confirmed to have COVID-19 during an outbreak can be challenging, as each study is lengthened and complicated by the need for strict adherence to infection control protocols designed to minimize risk of transmission and protect healthcare personnel (12). Droplet transmission followed by contaminated surfaces are believed to be the main modes of spread for SARS-CoV2 in radiology suites; all patients undergoing imaging should be masked and imaged using dedicated equipment that is cleaned and disinfected after each patient encounter (13).
Although personal protection equipment (PPE) recommendations vary between countries, the current Centers of Disease Control (CDC) guidelines recommend radiology staff wear a mask, goggles or face shield, gloves, and an isolation gown. In countries with more stringent PPE protocols, a surgical cap and shoe covers may be added, while a surgical mask and goggles or face shield are suggested in some countries with less stringent PPE protocols (14). Additional precautions are required for specific situations that are more likely to generate aerosols, including patients receiving non-invasive ventilation, during intubation or extubation, throughout bronchoscopy, or when receiving nebulized therapies. Portable imaging, including imaging patients through glass walls, has been used in some hospitals to further reduce the chance of spreading infection.
Written from multidisciplinary and multinational perspectives, this Fleischner statement is intended to provide context for the use of imaging to direct patient management during the COVID-19 pandemic in different practice settings, different phases of epidemic outbreak, and environments of varying critical resource availability. This document is structured around three clinical scenarios and three additional situations in which chest imaging is often considered in the evaluation of patients with potential COVID-19 infection. The committee elected to present this document as a consensus statement rather than a guideline given the limited evidence base and the urgent need for direction on this topic for the medical community. The final document was supported by a comprehensive literature search for relevant articles.

This
Using the search terms "((coronavirus OR COVID OR SARS-CoV OR *nCoV*) AND (CT OR Computed Tomography OR Radio* OR Imag*))", a total of 137 English articles published between Dec 1, 2019 and March 23, 2020 were identified. Each article was assessed for relevance to the primary objective and a summary of key findings from relevant articles was created.

The Use of Imaging in COVID-19
The value of an imaging test relates to the generation of results that are clinically actionable either for establishing a diagnosis or for guiding management, triage, or therapy. That value is diminished by costs that include the risk of radiation exposure to the patient, risk of COVID-19 transmission to uninfected healthcare workers and other patients, consumption of PPE, and need for cleaning and downtime of radiology rooms in resource-constrained environments.
The appropriate use of imaging in each of the scenarios was considered on this basis.
This statement focuses exclusively on the use of chest radiography (CXR) and computed tomography of the thorax (CT). While ultrasound has been suggested as a potential triage and diagnostic tool for COVID-19 given the predilection for the disease in subpleural regions, there is limited experience at this time (16), as well as infection control issues.

Scenario 1: Mild Features of COVID-19
The first scenario (Fig. 1) (Fig, 1, Q1). Imaging provides a baseline for future comparison, may establish manifestations of important comorbidities in patients with risk factors for disease progression ( Table 1), and may influence the intensity of monitoring for clinical worsening. Imaging is not advised for patients with mild features who are COVID-19 positive without accompanying risk factors for disease progression, or for patients with mild features who are COVID-19 negative (Fig. 1, Q2 & Q3). The panel felt that the yield of imaging in these settings would be very low and that it was safe for most patients to self-monitor for clinical worsening. Regardless of COVID-19 test results and risk factors, imaging is advised for patients with mild clinical features who subsequently develop clinical worsening (Fig, 1, Q4 & Q5). In the absence of clinical worsening, management involves support and isolation of patients with positive COVID-19 testing or patients with moderate to high pre-test probability without COVID-19 test results available.
Although not specifically addressed by this scenario, in the presence of significant resources constraints, there is no role for imaging of patients with mild features of COVID-19.

Scenario 2: Moderate to Severe Features of COVID-19
The second scenario (Fig. 2) addresses a patient presenting with moderate-to-severe features consistent with COVID-19 infection, any pre-test probability of COVID-19 infection, and no significant critical resource constraints. Separate ratings were obtained for COVID-19 positive patients and either COVID-19 negative patients or patients for whom COVID-19 testing is unavailable (Fig. 2, Q6 & Q7). Imaging is advised regardless of the results or availability of COVID-19 testing given the impact of imaging in both circumstances.
For COVID-19 positive patients, imaging establishes baseline pulmonary status and identifies underlying cardiopulmonary abnormalities that may facilitate risk stratification for clinical worsening. In the presence of clinical worsening, imaging is again advised to assess for COVID-19 progression or secondary cardiopulmonary abnormalities such as pulmonary embolism, superimposed bacterial pneumonia, or heart failure that can potentially be secondary to COVID-19 myocardial injury (Fig 2, Q8).

Environment
The third scenario (Fig. 3)  The third scenario first considers the potential availability of PoC COVID-19 testing. Imaging is advised when PoC COVID-19 testing is available and positive (Fig. 3, Q9) for the same reasons as described for Scenario 2. Based upon imaging findings and clinical features, patients are subsequently supported and monitored with a level of intensity consistent with clinical features. Imaging is again indicated if patients subsequently clinically worsen (Fig. 3, Q11).
Imaging is advised to support more rapid triage of patients in a resource-constrained setting when PoC COVID-19 testing is not available or negative (Fig. 3, Q10). Imaging may reveal features of COVID-19, which within this scenario may be taken as a presumptive diagnosis of COVID-19 for medical triage and associated decisions regarding disposition, infection control, and clinical management. In this high pre-test probability environment, and as described for Scenario 2, the possibility of falsely negative COVID-19 testing creates a circumstance where a COVID-19 diagnosis may be presumed when imaging findings are strongly suggestive of COVID-19 despite negative COVID-19 testing. This guidance represents a variance from other published recommendations which advise against the use of imaging for the initial diagnosis of COVID-19 (28) and was supported by direct experience amongst panelists providing care within the conditions described for this scenario. The relationship between disease severity and triage may need to be fluid depending upon resources and case load. When imaging reveals an alternative diagnosis to COVID-19, management is based upon established guidelines or standard clinical practice.
Additional Key Questions:

Daily chest radiographs are not indicated in stable intubated patients with COVID-19 (Q12)
Multiple studies have shown no difference in important outcomes (mortality, length of stay, and ventilator days) for intensive care unit patients imaged on-demand as compared to a daily routine protocol (29)(30)(31)(32). Avoidance of non-value-added imaging is particularly important in the COVID-19 patient population to minimize exposure risk of radiology technologists and to conserve PPE.

CT scan is indicated in a patient who has functional impairment and/or hypoxemia after recovery from COVID-19 (Q13)
With the recent emergence of SARS-CoV2 as a human pathogen, there are no long-term followup studies of survivors. Postmortem evaluation of a single patient who succumbed to severe COVID-19 showed pathologic findings consistent with diffuse alveolar damage, similar to findings previously described with severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) (33). Patients with functional impairment following recovery from COVID-19 should undergo imaging to differentiate between expected morphologic abnormalities as sequelae of infection, mechanical ventilation, or both versus a different and potentially treatable process.

COVID-19 on a CT scan. (Q14)
While CT findings of COVID-19 infection are nonspecific, their presence in an asymptomatic patient with no or mild respiratory symptoms is concerning in a setting of known community transmission, particularly if there is no better alternative diagnosis. Asymptomatic carriers of COVID-19 have been estimated to comprise 17.9% -33.3% of all infected cases (34,35).
Asymptomatic infection with suggestive CT findings in the lung has been documented in screened cruise ship passengers (11). It is believed that the presence of undetected infected and mildly symptomatic or asymptomatic individuals may be contributing to the rapid geographic spread of SARS-CoV2 (9). RT-PCR testing in this scenario is important to potentially identify an occult infection and limit further transmission both within the community and in the environment where the patient is receiving medical care. In highly prevalent areas, an additional uncertainty is whether CT should be used as a screening tool either as a stand-alone or as an adjunct to RT-PCR to exclude occult infection prior to surgery or intensive immunosuppressive therapies.
The panel's ratings are provided in Figure 4, and a summary of all recommendations is provided in Table 2.

Additional Resources
For purposes of image interpretation and reporting, readers are referred to a recently published systematic review of imaging findings of COVID-19 (36) and a multi-society consensus paper on reporting chest CT findings related to COVID-19 (37). As an aid to improving radiologist and pulmonologist familiarity with the imaging findings of COVID-19, we provide the following link (https://www.fleischner-covid19.org) to the Fleischner Society website where an educational repository of proven COVID-19 cases can be found.

Disease progression
• Progression of mild disease to moderate-to-severe disease as defined above.
• Progression of moderate-to-severe disease with worsening objective measures of hypoxemia.

Resource constraints
• Limited access to personnel, personal protective equipment, COVID-19 testing ability (including swabs, reagent, or personnel), hospital beds, and/or ventilators with the need to rapidly triage patients.