This report was approved by the institutional review board. Coronavirus disease (COVID-19), caused by infection with the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has rapidly spread around the world since the end of 2019.1–3 As of April 8, 2020, there are >1.43 million confirmed cases and 82,172 deaths around the world.4 In order to reduce the risks of SARS-CoV-2 transmission in the Radiology Department, the following represents a summary of actions that can be taken, although the strategies may vary among departments and institutions due to factors related to practice location, patient population, disease prevalence, and resource availability. All staff in the Radiology Department should be aware of the essential role he or she plays as a key member of the team to fight this deadly virus. Any loopholes in the prevention of spread of infection may compromise the availability of skilled personnel and the ability to provide patient care due to quarantine and hospitalization of staff or closure of an entire department. The insights learned during this difficult period will also be helpful to improve our collective preparedness for potential future episodes of widespread infectious illness.5–7
PREPAREDNESS OF RADIOLOGY DEPARTMENT
All staff, patients, and visitors of the Radiology Department should be encouraged to practice proper hand hygiene, which includes careful hand washing with soap for at least 20 seconds or hand sanitizer that contains 75% alcohol. Surgical masks should be worn by staff, patients, and visitors depending on local availability. The points of entry into the institution and Radiology Department should be limited for effective screening of patients, visitors, and employees, although employees should be screened separately.5–7 History of travel, occupation, contact, and cluster (TOCC) can be obtained before the visit or at the entry point. Body temperatures should be measured.5–7 Those suffering from symptoms of acute respiratory illness (eg, fever, cough, sore throat, generalized malaise, myalgia)3 or other recently reported symptoms of COVID-19, such as lack of appetite, vomiting, diarrhea,8 and/or anosmia,9 should be instructed to self-quarantine and/or directed to appropriate testing sites for SARS-CoV-2 infection based on local and institutional guidelines. Staff members with recent travel, contact with confirmed SARS-CoV-2 infected individuals, or contact with those having related symptoms should be instructed to self-isolate and contact employee health or their primary care physician for guidance. Staff members should not return to work until exclusion of potential infection or fulfillment of isolation period. A variety of social distancing measures should be taken to prevent clustering and ensure a distance of least 1.8 m or 6 feet between all individuals to reduce risk of infection. For busy Radiology Departments, depending on the local prevalence of COVID-19, imaging examination appointments may need to be reduced or scheduled with longer time intervals, and accompanying visitors should be limited to avoid crowding of the waiting areas.5–7
If possible, administrative staff should be encouraged and provided with resources, such as laptop computers and virtual private network connection, to work from home. If home workstations are available, radiologists, particularly those with risk factors for poor outcome if affected by COVID-19, should be allowed to work remotely to reduce potential exposure. Staff whose work requires in-person presence should have staggered shifts and work in fixed, small teams, and avoid any contacts with members outside of the assigned team. In the unfortunate event that 1 team member is suspected or confirmed to have COVID-19, only a relatively small number of team members that he or she has had contact with would need to be isolated. Members of other teams, without exposure, can continue to provide coverage of required functions. For departments that provide services at multiple locations, staff should remain at one location to the extent possible and avoid rotation to reduce the potential of cross-infection. For staff who work onsite, cleaning of the workstation, keyboards, mice, and other fomites should be performed at the start and end of each shift, and sharing by different staff members should be minimized. Staff should avoid congregating during coffee or meal breaks.5–7
All in-person meetings in the Radiology Department and institution should be canceled if possible. If a meeting is deemed necessary, limit the number of in-person participants to 6, at most. Various web-based social media and teleconference platforms (eg, Facebook, Webex, etc.) can be used for education, consultation, interdisciplinary conferences, or general communication.6,7
TRIAGE OF ESSENTIAL AND NONESSENTIAL EXAMINATIONS THAT CAN BE POSTPONED
Depending on the local prevalence of COVID-19, Radiology Departments may take a step-wise approach to postpone nonurgent imaging examinations and imaging-guided procedures.6,7,10,11 For example, screening mammography, nonemergent or nonessential interventional procedures, and low-dose computed tomography (CT) for lung cancer screening should be rescheduled, particularly because many of the patients, especially for lung cancer screening, have underlying cardiopulmonary abnormalities that can put them at increased risks for mortality from COVID-19 pneumonia. With increasing prevalence of infection, additional studies such as surveillance of treated malignancy, will need to be rescheduled. Decreasing the number of examinations and procedures will help prevent exposure of patients and staff to pathogens and free up resources such as CT scanners and personal protective equipment (PPE) to be used to evaluate and care for patients with suspected or confirmed SARS-CoV-2 infection.
PERFORMANCE OF CHEST RADIOGRAPHY FOR SUSPECTED OR CONFIRMED CASES OF COVID-19
Portable chest radiography (CXR) is the primary or initial imaging modality for assessing patients with suspected or confirmed COVID-19 pneumonia. Transfer of these patients to the Radiology Department is not recommended because of the risk of transmitting the infection en route and ease of disinfecting the portable unit.6,7,12
Setting up an isolated screening station with portable CXR outside of the emergency department is highly recommended. Digital radiography is superior to computed radiography due to its efficiency and lower risk of contamination.6 A special CXR examination code for COVID-19 is recommended so as to alert the technologist to wear necessary protection. This examination code will also be helpful to radiologists for efficient interpretation and later retrieving the images from the picture archiving and communication system for education.
The most frequent findings on radiographs are consolidations and ground-glass opacities (GGOs).13,14 The distribution is most often bilateral, peripheral, and lower zone predominant.14 In contrast to parenchymal abnormalities, pleural effusion is rare (3%).14 Of patients with COVID-19 requiring hospitalization, 69% had an abnormal chest radiograph at the initial time of admission, and 80% had radiographic abnormalities sometime during hospitalization.14 Findings are most extensive about 10 to 12 days after symptom onset.14 In nonsevere disease, up to 18% of patients have a normal initial CXR or CT, but only 3% in severe disease have normal CXR or CT.15 Deep learning tools can potentially improve detection and efficiency in the interpretation of these cases.16
PERFORMANCE OF CT FOR SUSPECTED OR CONFIRMED CASES OF COVID-19
CT of the chest is often requested by referring physicians for assessment of patients with respiratory symptoms to narrow the differential diagnosis, triage patients for admission, and to guide treatment decisions. Many of these patients may have suspected or confirmed COVID-19 pneumonia. Coordination with clinical services including emergency medicine, infectious disease, critical care medicine, pulmonary medicine, and, etc., to create the optimal institutional algorithm for evaluation to allow appropriate utilization of CT and notification of the Radiology Department before the arrival of patients with suspected or confirmed SARS-CoV-2 infection is critical.
Prerequisites of the CT Scanner Room
In areas where patients with suspected or confirmed COVID-19 are seen, one of 2 different algorithms should be used: one for a facility with a dedicated COVID-19 scanner, and the other for places without a dedicated CT scanner.5–7 If a dedicated CT scanner room is used, it should ideally not be too far away from the inpatient unit where patients with suspected or confirmed COVID-19 pneumonia are hospitalized, but the scanner room and the wards should not be on the same floor for fear of outbreaks in the ward.1,2,6,7 All unnecessary objects in the scanner room should be removed to minimize risk of contamination. The room should be equipped with ultraviolent rays or lamps to allow thorough disinfection. The ventilation system of the room, if possible, should be isolated from other patient care areas. When possible, mobile or portable chest imaging will be an optimal option to limit equipment, room, and hallway decontamination requirement.7
Creating a Safe Environment
The delivery of the CT services should be performed in a manner that maximizes safety for the radiology staff and the work environment.6,7,10 The waiting areas and the passageways between the inpatient unit and the CT room should be separate from the flow of traffic of other patients. Frequent communication between the referring service, radiology scheduling staff, and CT technologists is recommended to improve efficiency and minimize patient time in the CT room and exposure to radiology staff.
Scheduling and Arrangement of CT
If there are limited cases of suspicious or confirmed cases of COVID-19 at an institution, a dedicated CT scanner exclusive for COVID-19 may not be necessary. In this situation, optimal scheduling would be helpful.5–7 The CT schedule for suspicious or confirmed cases of COVID-19 pneumonia should be arranged at a time after all the routine CT examinations of the day have been completed. Patients with suspected COVID-19 pneumonia should be scheduled before the confirmed COVID-19 pneumonia patients.
Radiology Staff Preparation Before CT Examination
Before entering the CT scanner room, all subjects are required to wear surgical masks. Depending on the anticipated exposure, the staff must be aware of the appropriate usage of the PPE to avoid infection. Steps of putting on PPE: dry clean using 75% alcohol → first layer of gloves → gown → N95 mask → hair cap → face shield → second layer of gloves → shoes cover.17,18
Performance of CT Examination
- The Radiology Department staff should execute the examination according to the standard operating procedure (SOP). Before the patient is transferred to the examination room, the air conditioning should be turned off. Nonenhanced CT images are acquired at full inspiration during a single breath-hold with patients in the supine position, and the scanning field covers the entire thorax. The acquisition parameters are set at 120 kVp; 100 to 450 mA with automatic modulation; and pitch 0.75 to 1.5. All imaging data are reconstructed by use of a medium sharp reconstruction algorithm with a slice thickness of 1.0 mm, and a matrix of 512×512.19 Balance between minimizing radiation dose and optimal diagnostic image quality is needed to be considered.13
- Technologist A is responsible for positioning the patient and gantry control, and should be wearing appropriate PPE to avoid infection.
- Technologist B should not have direct contact with the patient, and is primarily responsible for console control, scan performance, and opening and closing of the inner and outer lead doors from the console operation room.
- CT technologists, fellows, and residents may receive a short education course in order to recognize typical appearance of COVID pneumonia, so that they will be able to report immediately or contact on-duty radiologists to prioritize interpretation of these images with major findings and trigger the SOP as early as possible. Free online COVID-19 educational resources are available on the websites of Journal of Thoracic Imaging and Society of Thoracic Radiology (https://journals.lww.com/thoracicimaging/pages/default.aspx and https://thoracicrad.org/, respectively). A web-based system (eg, TeleRad IT) is able to send CT images in consoles to radiologists at desired locations in real time, which can drastically improve the workflow efficiency. Artificial intelligence has been reported to be of help to radiologists in improving image interpretation and efficiency,20 especially during night shifts.
The staff in the Radiology Department play crucial roles in the disinfection measures. The following processes have been used according to the concept of triage, safety, and best practice to avoid contamination of staff, patients, and environment in view of the algorithm suggested by professional organizations.1,2,5,6
- After the patient leaves the CT room, technologist A inside the examination room is responsible for cleaning and disinfecting the gantry and its control panel with 75% alcohol first, → subsequently disinfect the examination table later with 500 ppm bleach solution.
- Technologist A should take off all PPE step by step in the following sequence18: with the gloves on, dry clean of hand with 75% alcohol (DC) → remove face shield and hang on the wall after disinfection with 500 ppm of bleach solution, which will be disinfected by UV light for at least 30 minutes → DC → remove hair cap → DC → remove gown and outer layer of gloves slowly from top to bottom by folding the inner part outwards to avoid contamination of environment→ DC → put tissue paper soaked with 500 bpm bleach solution nearby the outer door → remove shoes covers → DC → inner layer of gloves → DC → go outside the scanner room by standing on tissue paper soaked with 500 bpm bleach solution → put on new gloves → take off N95 mask outside the CT scanner room → remove gloves → hand wash with soap. Once the technologist A begins the process of disinfecting the CT gantry, the cleaning staff arranged by the institution will also come into the scanner room to disinfect the floor and the surrounding facilities. The cleaning staff should also be in appropriate PPE. Both cleaning staff and technologist A must take off all PPE after each patient’s examination, unless instructed otherwise due to shortage of PPE.
- The disposable PPE should be discarded into the biologic waste container. If the gown is not single-use, it should be discarded separately into a double layer plastic bag with a biohazard label attached. The contaminated gown should be cleaned and disinfected according to the SOP. The hazardous waste should be destroyed by incineration as per the institutional infection control protocols.
- The UV lamp should be turned on for disinfection for at least 30 minutes.
- Technologist B, who is in charge of operation console, should use 75% alcohol to disinfect the operating console and facilities outside the scanning room.
- The passageways between the inpatient unit and CT room should be disinfected according to the SOP after the procedure.
UNSUSPECTED PATIENTS WITH CT FINDINGS SUGGESTIVE OF COVID-19: EARLY DETECTION AND MANAGEMENT
A significant percentage of patients with COVID-19 may have no symptom or present with atypical symptoms. The estimated proportion of asymptomatic patients was 17.9% based on a recently published study.21 Therefore, it is possible to detect CT findings of COVID-19 pneumonia incidentally.22 In such scenarios, early identification and further management of these “unexpected COVID-19 patients” are critical. The preparedness and best practice for such cases include the following: (1) A temporary quarantine area in Radiology Department. (2) All staff members should put on, if not already wearing, facial masks, hair cap, and gloves. (3) On duty radiologist should be contacted immediately to review images to decide the probability of COVID-19 pneumonia. (4) If COVID-19 pneumonia is suspected, the radiologist should immediately notify the referring team, infection department, or emergency department depending on institutional protocol, or escort the suspected patient to the screening station if available at the institution. (5) Disinfect the CT scanner room and surrounding environment according to SOP.1,2,5,6
CT FINDING OF COVID-19 PNEUMONIA
Even though the American College of Radiology and the Society of Thoracic Radiology do not recommend routine CT screening for the diagnosis of patients under investigation for COVID-19, the practice varies in different parts of the world due to differences in the prevalence of the disease and availability of test kits. It is, nevertheless, imperative for radiologists to be familiar with the CT findings of COVID-19 pneumonia.
Lung abnormalities are more frequently identified on CT (Figs. 1A–D) in symptomatic cases than in asymptomatic ones, while asymptomatic cases show more GGO predominance over consolidation.23 Signs of pneumonia on CT can be seen in 54% and 80% of asymptomatic and symptomatic patients, respectively.23 In comparison with younger patients with corona virus disease, older patients are significantly more likely to have extensive lung lobe involvement, subpleural line, and pleural thickening on CT images.24 It is emphasized that up to 56% of patients may have normal CT within the initial 2 days of symptom onset.25
The CT findings may change rapidly from focal, unilateral, to diffuse bilateral GGOs that progress to or co-exist with consolidation, usually within 1 to 3 weeks.19,25–27 The lesions often demonstrate lower lung and peripheral predominance. Other imaging findings that usually occur later in the disease course include crazy-paving pattern, vascular thickening within the GGO, dilated airways, and the reverse halo or atoll signs suggestive of organizing pneumonia. Pleural effusion, small lung nodules, and lymphadenopathy may occur in a few cases and are likely associated with complications.26
In patients recovering from COVID-19 infection, 4 stages of evolution on chest CT have been described: early stage (0 to 4 d); progressive stage (5 to 8 d); peak stage (10 to 13 d); and absorption stage (≥14 d). In patients who recovered from COVID-19 pneumonia, initial lung findings on chest CT may be small subpleural GGOs that will become larger with consolidation and sometimes a crazy-paving pattern. Lung involvement may be increased by consolidation in up to 2 weeks after disease onset. After 2 weeks, the lesions will be gradually absorbed, leaving extensive GGOs and subpleural parenchymal bands.27
Despite the nonspecific findings, a recent publication28 reported that radiologists who participated in the study were able to distinguish COVID-19 from other viral pneumonia on chest CT with high specificity but moderate sensitivity.
Many radiology organizations such as the British Society of Thoracic Imaging (BSTI),29 the Radiological Society of North America (RSNA),30 and the Fleishner Society31 have provided tables and guidance to radiologists on the reporting of these cases.
According to the RSNA expert consensus statement30 endorsed by American College of Radiology (ACR), Society of Thoracic Radiology (STR), and RSNA, the typical CT features (Figs. 1A–D) include (1) peripheral, bilateral GGOs with or without consolidation or visible intralobular lines (crazy paving), or (2) multifocal GGOs of rounded morphology with or without consolidation or visible intralobular lines (crazy paving),32,33 or (3) reverse halo sign or other findings of organizing pneumonia (seen later in the disease). The indeterminate CT features (Figs. 1B, C) include absence of typical features AND (1) presence of multifocal, diffuse, perihilar, or unilateral GGOs with or without consolidation lacking a specific distribution and which are nonrounded or nonperipheral, or (2) few very small GGOs with a nonrounded and nonperipheral distribution. The atypical features are absence of typical or indeterminate features AND presence of (1) isolated lobar or segmental consolidation without GGOs (Fig. 1C), or (2) discrete small nodules (centrilobular, tree-in-buds), or (3) lung cavitation, or (4) smooth interlobular septal thickening with pleural effusion. The fourth category is negative for pneumonia when there are no features to suggest pneumonia. The statement also mentioned the rationale and proposed reporting language for CT findings related to COVID-19.
As the prevalence of COVID-19 pneumonia rapidly increases around the world, CT scans are increasingly being performed in patients with respiratory symptoms to help referring physicians differentiate COVID-19 pneumonia from other etiologies and triage patients for admission to the hospital due to wide availability of CT scanners.
CT AND REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION (RT-PCR) ASSAY
The positive rates of RT-PCR assay and chest CT imaging were reported to be 59% and 88% for the diagnosis of patients with suspected COVID-19, respectively. With RT-PCR as a reference, the sensitivity of chest CT imaging for COVID-19 is 97%. With analysis of serial RT-PCR assays and CT scans, 60% to 93% of patients had initial positive chest CT scans consistent with COVID-19 before the initial positive RT-PCR results. Forty-two percent of patients may show improvement of follow-up chest CT scans before the RT-PCR results turn negative.34 The false-negative rates of RT-PCR assays and chest CT in other countries with different prevalence of COVID-19 pneumonia remain to be determined, as a large number of different test kits are being used around the world. In confirmed cases proved by RT-PCR, CT had a sensitivity of 54% and 79% in asymptomatic and symptomatic patients, respectively.23
CLINICAL PREDICTORS OF POOR OUTCOME
Three major risk factors associated with death from coronavirus include older age, symptoms of sepsis, and elevated levels of blood fibrin degradation products. To be specific, the patients’ risk of death increased by 1.1 times for each year of age, by >5 times for those with a Sequential Organ Failure Assessment (SOFA) score high enough to indicate sepsis, and by about 18 times for those who had a D-dimer blood test score exceeding 1 µg/mL.35
A systematic review and meta-analysis of 30 studies on 53,000 patients with COVID-19 showed that the pooled incidence of severity and mortality were 20.2% and 3.1%, respectively.36 The predictors for disease severity included old age, male sex, smoking, and any comorbidity. Old age (60 y and above, relative risk or RR=9.45), followed by cardiovascular disease (RR=6.75), hypertension (RR=4.48), and diabetes (RR=4.43) were found to be independent prognostic factors for the COVID-19-related death. In terms of laboratory results, elevated levels of interleukin-6, troponin I, lactate dehydrogenase (LDH), C-reactive protein (CRP) and D-dimer, and decreased blood platelet and lymphocyte count were highly associated with severe COVID-19 (all for P<0.001).36
IMAGING SIGNS OF SEVERITY
According to the Chinese Guidelines for the Diagnosis and Treatment of New Coronavirus Pneumonia,37 the initial and follow-up CT features of patients with disease severity were analyzed. Of 73 patients, 6 (8%) patients were diagnosed as suffering from mild-type pneumonia; these patients had no or mild lung changes.38 All 43 (59%) patients with moderate type manifestations featured focal or multiple GGOs in the peripheral lungs, with or without interlobular septal thickening. In 21 patients (29%) with severe type, extensive GGOs or pulmonary consolidations were found. An extensive “white lung,” with atelectasis and pleural effusion, was found in 3 critical-type patients (4%).38
In a series of 42 patients, 35 (83%) patients exhibited progression of CT features.39 Follow-up CT findings showed progressive opacifications, consolidation, interstitial thickening, fibrous strips, and air bronchograms, compared with initial CT (all P<0.05). Before initiation of treatment, there was a moderate correlation between the days from onset and sum score of opacifications (R=0.68, P<0.01). The CRP, erythrocyte sedimentation rate, and LDH showed significantly positive correlation with the severity of pneumonia assessed on initial CT (R=0.36 to 0.75, P<0.05). The highest body temperature and the severity of opacifications assessed on initial CT were significantly related to the progression of opacifications on follow-up CT (P=0.001 to 0.04).39
The CT severity score (CT-SS) of 84 cases with mild and 18 cases with severe disease were studied.40 The CT-SS was defined by summing up individual scores from 20 lung regions; scores of 0, 1, and 2 were, respectively, assigned for each region if parenchymal opacification involved 0%, <50%, or ≥50% of each region, leading to a theoretical range of CT-SS from 0 to 40. The individual scores of each lung, as well as the total CT-SS, were significantly higher in severe COVID-19 when compared with mild cases. The optimal CT-SS threshold for identifying severe COVID-19 was 19.5 (area under curve, 0.892), with 83.3% sensitivity and 94% specificity. The severity of abnormalities quantified on chest radiographs in patients with severe acute respiratory syndrome correlates well with clinical parameters.41
In conclusion, the role of CXR and CT remain to be further defined as the world continues to fight the coronavirus pandemic. Radiology Departments can take measures to prevent the transmission of disease to protect patients and staff. Familiarity of radiologists with CXR and CT findings of COVID-19 pneumonia is essential in providing optimal care to patients with respiratory symptoms.
SUMMARY AND LEARNING POINTS
- Execution of TOCC and limitation of points of entry into the institution and Radiology Department allows optimal screening, isolation, and triage of staff and patients.
- Social distancing measures such as reducing number of imaging examinations, in-person meetings, and working remotely help protect staff and patients from exposure and potential need to quarantine.
- Imaging of patients with suspected or confirmed COVID-19 should be performed with appropriate use of PPE and implementation of disinfection procedure in the Radiology Department. The roles of two technologists in performing CT is critical for the safety of staff and patients as well as avoiding contamination of environment and facilities.
- CT can be abnormal in asymptomatic patients but may be normal in symptomatic patients particularly in the early stage of disease. The typical CT findings of COVID-19 pneumonia include peripheral, bilateral, multilobar GGOs with or without consolidation or crazy paving, and multifocal GGOs of rounded morphology with or without consolidation or crazy paving.
- Preparedness and best practice should be in place to quickly identify and isolate patients with incidentally detected CT findings suspicious for COVID-19.
- The extent and severity of CT findings of patients with COVID-19 correlated with severity in clinical classifications. The risk factors for severe illness or poor outcome are older age (especially with comorbidities), symptoms of sepsis, and elevated levels of interleukin-6, troponin I, LDH, CRP, and D-dimer, and decreased blood platelet and lymphocyte counts.
The authors appreciate Dr Dinah Wan, Southlake Plastic Surgery, Texas, and Dr Patricia W. Wu, Department of Medical Imaging and Intervention, Linkou Chang Gung Memorial Hospital, Taiwan, for their assistance in revising this manuscript. The authors are also grateful to all colleagues for their effort in preventing the hospital outbreak of COVID-19.
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