key: cord-0730474-cjjy68sb
authors: Lang, Min; Som, Avik; Carey, Denston; Reid, Nicholas; Mendoza, Dexter P.; Flores, Efren J.; Li, Matthew D.; Shepard, Jo-Anne O.; Little, Brent P.
title: Pulmonary Vascular Manifestations of COVID-19 Pneumonia
date: 2020-06-18
journal: Radiol Cardiothorac Imaging
DOI: 10.1148/ryct.2020200277
sha: a9ab9280979260d8fd30cd289bfeb05f3890cdc6
doc_id: 730474
cord_uid: cjjy68sb

BACKGROUND: Parenchymal findings in COVID-19 pneumonia on computed tomography (CT) have been well characterized. However, the role of pulmonary vascular pathology in COVID-19 pneumonia is still not well understood. PURPOSE: To investigate pulmonary vascular abnormalities on CT pulmonary angiography in patients with COVID-19 pneumonia. MATERIALS AND METHODS: In this retrospective study, 48 patients with RT-PCR confirmed COVID-19 infection who had undergone CT pulmonary angiography between 3/22/20 and 4/5/20 in our large urban health care system were included. Patient demographics and clinical data were collected through the electronic medical record system. Twenty-five patients underwent dual energy CT (DECT) as part of the standard CT pulmonary angiogram protocol at a subset of the hospitals. Two thoracic radiologists independently assessed all studies. Disagreement in assessment was resolved by consensus discussion with a third thoracic radiologist. RESULTS: Of the 48 patients, 45 patients required admission, with 18 admitted to the ICU, and 13 requiring intubation. Seven patients (15%) were found to have pulmonary emboli. Dilated vessels were seen in 41 cases (85%), with 38 (78%) and 27 (55%) of cases demonstrating vessel enlargement within and outside of lung opacities, respectively. Dilated distal vessels extending to the pleura and fissures were seen in 40 cases (82%) and 30 cases (61%), respectively. On DECT, mosaic perfusion pattern was observed in 24 cases (96%), regional hyperemia overlapping with areas of pulmonary opacities or immediately surrounding the opacities were seen in 13 cases (52%), opacities associated with corresponding oligemia were seen in 24 cases (96%), and hyperemic halo was seen in 9 cases (36%). CONCLUSION: Pulmonary vascular abnormalities such as vessel enlargement and regional mosaic perfusion patterns are common in COVID-19 pneumonia. Perfusion abnormalities are also frequently observed at DECT in COVID-19 pneumonia and may suggest an underlying vascular process.

Since December 2019, infection by novel coronavirus SARS-CoV-2 has erupted into a global pandemic, with more than 2.3 million reported cases worldwide to date.(1) The parenchymal imaging findings of COVID-19 pneumonia have been well described, including multifocal peripheral ground glass opacities with or without consolidation. (2) (3) (4) (5) However, these findings are not specific and can be seen in various other diseases including other viral pneumonias, atypical bacterial pneumonia, drug toxicity, eosinophilic pneumonia, or cryptogenic organizing pneumonia. (3, (6) (7) (8) I n p r e s s 4 Progression to acute respiratory distress syndrome (ARDS) has been reported in 20% of COVID-19 pneumonia cases and in up to 41% in patients who are hospitalized. (9) However, some patients requiring intubation have relatively preserved lung compliance, suggesting involvement of other processes in addition to parenchymal damage. Recent studies have proposed that loss of perfusion regulation and loss of normal physiologic hypoxic vasoconstriction contribute to the hypoxemia seen in patients with COVID-19. (10, 11) In addition, there has been increasing concern for hypercoagulability and pulmonary embolism (PE) in patients with COVID-19, with a few concordant autopsy studies reporting findings of pulmonary microthrombi. (12) (13) (14) (15) (16) (17) Finally, regional and diffuse pulmonary vascular pathology has also been suggested, including conditions mimicking high-altitude pulmonary edema. (18) Consistent with vascular pathology playing an important role in the pathophysiology of COVID-19 pneumonia, prior reports did note a high prevalence of vessel enlargement and thickening within areas of pulmonary parenchymal opacity in patients with COVID-19. (2, 4, 5) However, to our knowledge, a detailed investigation of pulmonary vascular findings on CT is lacking in the literature.

Recently, we observed perfusion abnormalities in several patients with COVID-19 infection who underwent dual energy CT (DECT) imaging for suspicion of pulmonary emboli. (19) These perfusion changes further support an underlying vascular pathology, but systematic investigation of its manifestation in COVID-19 pneumonia has not been described. Our goal was to assess pulmonary vascular findings on CT, including the prevalence of PE in our cohort, abnormalities of pulmonary vessels and mosaic attenuation. In addition, we used dual energy CT (DECT), available on a subset of our scanners, to obtain pulmonary blood volume (PBV) images and assess lung perfusion patterns in COVID-19 pneumonia.

This retrospective study was performed at the Partners HealthCare system, a large, quaternary academic medical center. This study was approved by the Institutional Review Board with a waiver of informed consent, and patient privacy was ensured in compliance with the Healthcare Information Portability and Accountability Act. All procedures and practices were in accordance with the Declaration of Helsinki.

I n p r e s s 5 Between March 23 and April 6, 2020, 353 computed tomography pulmonary angiography (CT-PE) studies were completed across the Partners HealthCare system for patients in an inpatient or emergency room setting. Of these patients, 51 had a positive reverse transcriptase polymerase chain reaction (RT-PCR) analysis for COVID-19 infection via nasopharyngeal swab at any point during their stay in the hospital or emergency department and were included in this retrospective study. The time range between the RT-PCR test and CT-PE study was 0 to 14 days, with RT-PCR always performed on the same day or preceding the CT-PE study. Three patients with nondiagnostic CT-PE studies were excluded from the study due to excessive motion. The remaining 48 patients were included in this study. Patient demographics, date of admission, comorbidities, clinical course, laboratory findings were retrospectively collected through our electronic medical record system.

All images were obtained with patient in the supine position using one of the following CT systems: Discovery CT750 HD (GE, America), Revolution Frontier (GE, America), SOMATOM Definition Flash (Siemens Healthineers, Germany), SOMATOM Definition AS (Siemens Healthineers, Germany), SOMATOM Force (Siemens Healthineers, Germany), and Aquilion ONE (Toshiba, Japan). The main scanning parameters were: tube voltage = 140 kVp (plus 80 kVP for dual energy), matrix = 512 × 512, slice thickness = 1.25 mm, field of view = 440 mm × 440 mm. CT imaging was not used for screening or primary diagnosis of COVID-19 at our institution but was used to assess potential complications or help guide clinical management in difficult cases.

CT-PE images for all patients were retrospectively and independently analyzed by two thoracic radiologists (11 years and 2 years of thoracic imaging subspecialty experience) using standard PACS viewing software and standard viewing windows. Disagreement in CT scoring and categorization of CT patterns was resolved by consensus discussion with a third thoracic radiologist (7 years of subspecialty experience). All radiologists were blinded to the original radiology report and to clinical and laboratory findings.

All studies were evaluated for presence of ground-glass or consolidative opacities, predominant distribution of opacities (peripheral -distal 1/3 of the lung, central -central 2/3 of the lung, or diffuse). Each lobe was also graded quantitatively on a severity score for opacities I n p r e s s 6 ranging from 0 to 4 (0=none, 1=1-25%, 2=26-50%, 3=51-75%, 4=76-100%), and a total severity score was calculated by summing the scores of all 5 lobes.

The images were categorized based on the RSNA/STR/ACR reporting guidelines, as either having "no evidence of pneumonia", an "atypical appearance", an "indeterminate appearance", or a "typical appearance" for COVID-19 pneumonia. (20) Briefly, these guidelines note that a "typical appearance" is characterized by having any of the following, including peripheral bilateral ground-glass opacities with or without consolidation or intralobular lines, multifocal ground glass opacity with rounded morphology with or without consolidation, or a reverse halo sign.

"Indeterminate findings" were defined as having the absence of typical features, and any of the following features, including: presence of ground glass opacities with or without consolidation in a non-rounded morphology that can be in a non-peripheral, perihilar or diffuse distribution. In addition, cases with a few small ground glass opacities with a non-rounded morphology and nonperipheral distribution constituted "indeterminate" findings per the RSNA reporting guidelines. Further, an "atypical appearance" was defined as the absence of typical or indeterminate features, with presence of either lobar/segmental consolidation without ground glass opacities. Additional findings including discrete centrilobular nodules, lung cavitation, or smooth interlobular septal thickening with pleural effusion were also categorized as features of "atypical appearance". If there were no CT findings to suggest pneumonia, the CT was assigned the category of "negative for pneumonia".

All CT-PE images were evaluated for presence of PE and pulmonary infarct (such as wedge shaped ground glass opacities), main pulmonary artery diameter, and evidence of right heart strain (right ventricle : left ventricle short axis > 1 ).(21) Additional parameters recorded on CT Lung window (Hounsfield units: -500 to 1000) include presence of reverse halo sign, presence of septal thickening, emphysema, centrilobular nodules, or bronchial wall thickening. In addition, radiologists evaluated the pulmonary vasculature specifically for the following signs: vessel enlargement within areas of parenchymal opacity, vessel enlargement outside of opacities, dilated distal subsegmental vessels touching pleura or fissures, and mosaic attenuation pattern (areas of more lucent/oligemic lung adjacent to areas of disease lung) in areas of the lung outside of the pulmonary opacities. Vessel enlargement was defined as vessel diameter larger than expected for the point within the vascular tree, characterized by 1) vessel diameter larger than that in adjacent portions of non-diseased lung, 2) vessel diameter larger than that in comparable regions of non-I n p r e s s 7 diseased contralateral lung, or 3) focal dilation or non-tapering of vessels as they course toward the lung periphery.

DECT were performed on 25 patients. These images were qualitatively assessed for mosaic perfusion (areas of heterogeneity on the pulmonary blood volume [PBV] images with alternating relatively higher and lower perfusion), focal hyperemia (areas of relative increase in perfusion compared to background lung), focal oligemia (areas of relative decrease in perfusion compared to background lung), and presence or absence of a rim of increased perfusion around an area of low perfusion (compared to background lung) corresponding to a parenchymal opacity -a "hyperemic halo" sign.

Normally distributed data was presented as mean (SD), non-normally distributed data as median (IQR), and categorical variables as frequency (%). Confidence intervals (CI) of proportions were calculated. Spearman-rho correlation coefficients were used for correlation between variables, and kappa inter-rater variable was used for statistical analysis of normally distributed data was presented as mean (SD), non-normally distributed data as median (IQR), and categorical variables as frequency (%). Spearman rank correlation was used to evaluate nonparametric, nonlinear data and Pearson correlation was used to evaluate continuous normally distributed data. P value less than 0.05 was set as statistical significance. Statistical analysis was performed using Prism (Graphpad, San Diego, CA), RStudio (RStudio, Boston, MA) and Stata (StataCorp, College Station, TX).

A total of 48 patients were included in this retrospective study. The average age was 58 ± 19 years and 23 patients (48%) were female ( Table 1 ). The most common presenting symptoms include cough (71%), fever (60%), and shortness of breath (58%). Hypertension (48%), obesity (44%), history of malignancy (23%), and diabetes (19%) were the four most prevalent comorbidities. No patients had prior liver disease. Only two (4%) patients had a pre-existing pulmonary condition of chronic obstructive pulmonary disease (COPD). Six (13%) patients had a history of pulmonary embolism. Forty-five patients (94%) required admission, with 18 patients (38%) requiring admission to the intensive care unit (ICU). Thirty-five patients (73%) required I n p r e s s 8 nasal cannula to maintain oxygen saturation above 90% during the admission, with 13 patients (27%) of these patients eventually requiring intubation. At the date of last follow up, 14 patients were discharged (29%) and 2 patients who required intubation were deceased (4%).

Consistent with previous reports, the most common features seen on chest CT of patients with COVID-19 are multilobar ground-glass opacities with or without consolidation in a predominantly peripheral distribution (Table 2) ; of note, the distribution was assessed in 44 cases, as 4 studies were categorized as "negative for pneumonia" without evidence of opacity. The average severity scores of individual lobes are listed in Table 2 and were significantly different between the lobes (P = 0.03), with both lower lobes having a higher average severity score (average left lower lobe severity score of 1.9 out of 3, and average right lower lobe severity score 2 out of 3) than the other lobes (range 1.3-1.7 out of 3) ( Table 2 ). Based on the RSNA/STR/ACR consensus guideline the findings were classified as "typical" in 55% of cases, "indeterminate" in 22%, "atypical" in 13%, and negative for pneumonia in 8% (Table 2) .

A total of 7 patients (15%) were found to have PE (supplemental Figure 1) , with 6 cases (13%) involving arteries of multiple lobes, 3 cases (6%) exhibited pulmonary infarcts, and 1 case (2%) with evidence of right heart strain ( Table 3) (Table 3 ; 6136 ± 3951 ng/mL vs 3653 ± 1439 ng/mL, respectively; P = .02).

Overall, dilated pulmonary vasculature was seen in 41 (85%) of cases, with 38 (79%) within pulmonary opacities and 27 (56%) outside of the opacities (Table 3, Figure 1A , 2, & 3C), and dilated distal pulmonary vessels extending to the pleura and fissures were seen in 40 cases (83%) and 30 cases (63%), respectively ( Figure 4A -B, 5). As described, vascular enlargement was often within or outside the opacity, and extended to the pleura generally near ground-glass opacities without diffuse involvement. Ten of our patients had chest CT imaging available that was performed within 6 months prior to COVID-19 infection and none of the vascular findings or evidence of pulmonary hypertension were observed previously. Mosaic attenuation, likely from mosaic perfusion, was noted in 45 cases (94%) on conventional chest CT lung window (Hounsfield units: -500 to 1 000). Dilated pulmonary vessels even outside of vessels with emboli were seen in 5 out of 7 patients with PE.

Overall, dual energy CT was performed in 25 cases (52%). A mosaic perfusion pattern was observed in 24 cases (96%) with 1 (4%) categorized as mild, 17 (68%) as moderate, and 6 (24%) I n p r e s s 9 as severe (Table 4 ; Figure 1B&D , 2B&D, 3B&D). More specifically, regionally increased hyperemia overlapping with areas of pulmonary opacities or immediately surrounding the opacities were seen in 13 cases (52%). Pulmonary opacities associated with corresponding oligemia on DECT were observed in 24 cases (96%). Intensely hyperemic area surrounding oligemic pulmonary opacities forming a peripheral "hyperemic halo" was noted in 9 cases (36%).

Of note, all 7 patients with PE exhibited perfusion abnormalities on DECT -7 had mosaic perfusion, 4 had hyperemia overlapping with areas of pulmonary opacities, 7 had oligemia, and 4 had hyperemic halo. Supplemental Figure 2 provides a reference of normal conventional chest CT and DECT images in a patient with COVID-19 infection but without respiratory symptoms and without lung parenchymal abnormalities on imaging; CT pulmonary angiogram was obtained for chest pain, tachycardia, and elevated D-dimer. Finally, of the 25 patients that underwent DECT, perfusion abnormalities were seen in all patients that required intubation or were deceased (4 of 4 patients) and in 95% of patients that did not require intubation (20 of 21 patients).

The pulmonary response to pneumonia is generally characterized by hypoxic pulmonary In normal lung, distal subsegmental vessels are usually inconspicuous within the subpleural regions. A substantial number of patients in our study, however, exhibited dilated and sometimes tortuous distal vessels in the subpleural lung. This phenomena is distinct from the pulmonary vascular thickening (or the "thick vessel sign") within pulmonary opacities in COVID-19 pneumonia that has been reported to range from 59% to 82% in patients with COVID-19. (2, 4, 5) This finding is nonspecific and can be seen in conditions such as pulmonary hypertension, I n p r e s s 10 pulmonary venous hypertension, pulmonary veno-occlusive disease, hepatopulmonary syndrome and portopulmonary hypertension. (27) However, patients in this study with imaging prior to COVID-19 infection had none of these findings, which argues against a chronic process.

Moreover, there was a lack of hepatic disease or other pre-existing pulmonary conditions that would provide a reason for the vascular pathology. DECT is a powerful imaging tool used to characterize pulmonary blood volume and patterns of pulmonary perfusion by taking advantage of the different attenuation profiles of different substances. (39, 40) This is achieved by utilizing two different X-ray energy spectra concurrently during imaging. DECT is part of the standard pulmonary embolus CT protocol at a subset of hospitals within our healthcare system. In the COVID-19 setting, DECT may provide insight into physiologic process of vascular shunting. Out of the 25 patients who underwent DECT in our study, mosaic perfusion abnormalities were seen in 24 patients (96%), with predominately increased perfusion proximal to areas of lung opacities. Mosaic perfusion is a subset of mosaic attenuation and can be broadly categorized into two etiologic categories: small airway disease with hypoxemic vasoconstriction due to air trapping, or small vessel disease. (40, 41) While mosaic I n p r e s s 11 attenuation and perfusion can be seen in infections because of diffuse airway abnormalities and/or mucus plugging, the perfusion changes in our patients did not correlate in most cases with bronchial wall thickening, visible secretions, mucous plugging, or emphysema, arguing against small airway disease as a sole or primary underlying cause. Furthermore, the perfusion abnormalities had a regional rather than lobular distribution and extended beyond areas of parenchymal lung opacity, suggesting the possibility of a diffuse vascular process.

There were decreased areas of peripheral perfusion corresponding to peripheral lung opacities in 24 out of 25 patients who underwent DECT (96%). This radiographic observation can be consistent with ARDS as areas of oligemia can be seen in ARDS related thrombosis. (33) The opacities with corresponding decreased perfusion may represent filling of airspaces and interstitium with exudates, or possibly peripheral areas of infarction mediated by small vessel thrombosis. Furthermore, of the 25 patients that underwent DECT, perfusion abnormalities were observed in all patients that required intubation or were deceased, and in 95% of patients who did not require intubation. This suggests that perfusion abnormalities are highly prevalent in symptomatic patients who required admission. The small number of patients who underwent DECT, however, limited meaningful correlation of these findings to degree of hypoxemia or clinical outcome, which will require further investigation. Interestingly, however, there was a peripheral halo of increased perfusion surrounding peripheral opacities in 9 patients (36%). This appearance is not typical in ARDS or acute or chronic pulmonary embolism, in which uniformly decreased perfusion is seen within affected areas. The peripheral halo of increased perfusion observed in our study has neither been described in the literature nor noted in our practice in cases of pulmonary infarction due to bland pulmonary emboli, but has been described once previously in a case of bacterial pneumonia. (40) This suggest an interplay between inflammatory processes and vascular phenomena in a subset of COVID-19 pneumonia. Further research into whether dual energy CT may provide prognostic information for patients with COVID-19 is needed.

There are multiple possible causes of differential pulmonary perfusion. Pulmonary embolism, pulmonary hypertension, and vasculitis are additional conditions that can alter pulmonary perfusion.(42) PE and pulmonary hypertension as the primary underlying causes of mosaic perfusion in our cohort of patients with COVID-19 pneumonia are unlikely given that perfusion abnormalities were seen in patients without visible PE and often did not correspond to areas supplied by the pulmonary arteries containing thrombus; furthermore, our patients did not have a history of pulmonary hypertension and only a small proportion of patients exhibited a mildly dilated main pulmonary artery (17%). Vasculitis secondary to infection can have varying I n p r e s s 12 appearances on imaging, including vessel wall thickening, cavitary lesions, and ground glass or consolidative opacities. (43) However, it would be unusual for isolated involvement of medium to small pulmonary vessels and there is a lack of concordant findings reported on pathology. (13, 16) There has been suggestion that the pathophysiology underlying COVID-19 pneumonia may resemble high altitude pulmonary edema (HAPE). (18) While there are imaging similarities including patchy ground glass opacities, dilated vasculature and regional perfusion changes, (44) (45) (46) ) the fundamental mechanism may be different, as COVID-19 is likely inflammatory mediated whereas HAPE is characterized by uneven pulmonary vasoconstriction, increased pulmonary artery pressure and endothelial leakage. (47) Abnormal inflammatory mediated vasodilatory response in COVID-19 pneumonia may result in intrapulmonary shunting toward areas of impaired gas exchanged and worsening of ventilation-perfusion mismatch, possibly explaining the enlarged vessels leading to and within areas of parenchymal opacity seen in our study.

The theory that patients with COVID-19 are at higher risk of both venous and arterial thrombosis has also recently garnered attention. The reported risk of venous thromboembolism in patients with COVID-19 has been reported to range from 25% to 31%. (12, 14) The incidence of PE specifically have been reported to range from 14% to 30%. (12, 15, (48) (49) (50) Similarly, 7 patients (15%) in our study were found to have PE, four of whom had risk factors including history of arrhythmia, malignancy, or prior PE or DVT. Acute PE, therefore, may be a potential concern in patients with COVID-19 similar to other viral pneumonias and critically ill patients in general. (51) (52) (53) In addition to medium to large vessel thrombosis, a handful of autopsy reports of COVID-19 have reported findings of microthrombosis and small vessel thickening, which can be seen in the setting of acute respiratory distress syndrome (ARDS), coagulopathies, other etiologies of vessel injury. (13, 16, 54) Our study had several limitations. The study was retrospective, and the patient cohort size is relatively small given our inclusion criteria of COVID-19 patients who underwent pulmonary CT angiography during a two-week window. Most patients in the study did not have a recent prior chest CT that would allow us to assess the temporal development of image findings, and it is possible that some of the vascular abnormalities predated the CTs obtained during the acute illness.

Many of the findings we detected are nonspecific and can occur in other diseases, and our study was not designed to assess the specificity of the findings for COVID-19 pneumonia. DECT images were only available for 25 patients due to availability of scanners at different hospital across our healthcare system and inspiratory and expiratory phases were not performed as part of the standard imaging protocol, which may potentially confound mosaic patterns seen on CT images. Our study I n p r e s s 13 is also limited by the lack of control groups -patients without COVID-19 infection or those with COVID-19 infection but who did not require admission. Future studies with matched control groups, as well as patients with other appropriate pathologies, including organizing pneumonia and influenza, would be helpful to further clarify the extent of these vascular findings. Finally, assessment of vessel enlargement and mosaic perfusion can be subjective, and therefore requires further confirmation with larger multi-reader studies or quantitative methods of categorization.

In conclusion, COVID-19 pneumonia appears to be associated with pulmonary vascular and pulmonary perfusion derangements that are caused by unclear mechanisms. Pulmonary vessel dilatation occurs not only within lung opacities, but also occurs in a regional pattern outside of parenchymal opacities, and sometimes involves the subpleural lung. Perfusion abnormalities are also frequently seen on DECT imaging. Further imaging and pathologic studies are required to investigate the possible contributions of abnormal vasoregulation, intrapulmonary shunting, and/or microvascular thrombosis.

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I n p r e s s 17 (A-B) 41-year-old male who presented to the emergency room with acute shortness of breath and underwent pulmonary CT angiography for concern for pulmonary embolism. Patient tested positive for COVID-19 infection. A) Peripheral ground glass opacities are present in the posterior upper lobes (arrowheads); regional dilation of vessels is noted in adjacent upper lobes (arrows). B) Pulmonary blood volume (PBV) image at the same level shows peripheral perfusion defects corresponding to the opacities, with surrounding halos of increased perfusion (arrowheads).(C-D) 57-year-old female who presented with 7 days of fever, malaise, chills, cough, and increasing shortness of breath. On day 3 of admission, patient developed increasing oxygen requirement and elevated D-dimer level. C) CT of the upper lungs at lung windows shows ground glass opacities in the central and peripheral upper lungs bilaterally, with regional low attenuation of a portion of the right upper lobe and superior segment of the right lower lobe (arrowheads). Vessels within the low attenuation region are diminutive in a regional pattern, while vessels in the areas of ground glass opacity are dilated (arrows). D) Corresponding iodine map image shows regional decreased perfusion to the right lung (white arrowheads) and increased perfusion to the areas of ground glass opacity, while there is also heterogenous perfusion of the left upper lobe.I n p r e s s 23 Figure 4 . A-B) 47-year-old female with a history of metastatic breast cancer initially presented with nausea, vomiting, and low-grade fever and tested positive for COVID-19 infection. Patient underwent CT pulmonary angiogram on day 4 of admission for acute intermittent tachycardia, lethargy, and new oxygen requirement. A) Axial CT image with lung windows through the left lower lobe at time of presentation shows abnormally dilated distal subsegmental vessels in the subpleural lung touching the pleural surface (arrowheads). B) Image at the same level of a CT of the same patient 11 days prior shows normal vessel sizes and appearances, with a normal appearance of the subpleural lung.C-D) 64-year-old male presented with acute onset of fatigue, headache, cough, fever, and shortness of breath and tested positive for COVID-19. On day 12 of admission, patient develop increasing oxygen requirement and CT pulmonary angiogram was performed. C) Axial CT image with lung windows through the right lower lung shows peripheral regional ground glass opacity in the right lower lobe, with dilated segmental and subsegmental vessels supplying the region of opacified lung (arrows) and smaller diameters of vessels in unaffected lung (arrowheads). D) Image at the same level of a CT of the same patient approximately 3 months prior shows normal appearance of vessels. I n p r e s s 24 Figure 5 . A) 84-year-old female with a history of breast cancer who presented to the emergency room for fever, weakness, altered mental status, acute shortness of breath, and chest pain, for which pulmonary angiogram was obtained. Axial CT image shows dilated, non-tapering, tortuous vessels in the posterior right lower lobe (arrowheads), some of which extend to the pleural surface. B) A CT of the same patient shown at the same level five months prior shows normal vessels. C) 27year-old female who presented to the emergency room with acute shortness of breath and dyspnea on exertion. Patient was subsequently found to be COVID-19 positive and worsening tachypnea. Axial CT image through the lower lobes shows multiple dilated tortuous vessels within the lower lobes, with extension to the pleural surfaces (arrowheads). 22-year-old with COVID-19 and normal chest CT. A) Axial CT image with lung windows shows clear lungs and normal vascularity; there is normal lack of visualization of vessels in the subpleural lung. B) Corresponding pulmonary blood volume (PBV) image from the same examination shows normal pulmonary blood volume distribution, with a mild smooth gravitational gradient favoring the posterior lungs, and no focal perfusion abnormalities.