Acta Radiol 2013 Casullo 505 10

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DOI: 10.1177/0284185113475797

2013 54: 505 originally published online 30 April 2013Acta RadiolJoseph Casullo and Alexandre Semionov

Reversed halo sign in acute pulmonary embolism and infarction

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Original article

Reversed halo sign in acute pulmonary embolism and infarction

Joseph Casullo and Alexandre Semionov

Department of Diagnostic Radiology, Montreal General Hospital, McGill University Health Center, Montreal, Quebec, Canada

Correspondence to: Joseph Casullo. Email: [email protected]

AbstractBackground: The reversed halo sign, originally described in cryptogenic organizing pneumonia, has

been observed in a variety of pulmonary diseases, including pulmonary embolism (PE).

Purpose: To describe the computed tomographic (CT) findings in patients with the reversed halo sign

and acute PE at initial presentation and in subsequent scans.

Material and Methods: Contrast-enhanced CT examinations of 12 patients with the reversed halo sign

and acute PE were analyzed retrospectively. The diagnosis of pulmonary embolism was made by CT

angiography in 11 cases and by a routine contrast-enhanced scan of the chest in the other case.

Follow-up scans of seven patients and follow-up radiographs of two patients were also examined

retrospectively. The average age of the patients was 49 years (range, 2180 years). Seven (58%) patients

were women. Six patients had no significant medical history, and six patients had deep venous thrombosis

initially.

Results: The reversed halo sign was observed as a single lesion in 10 patients; in two patients, two

lesions were found. The lesions, all pleural-based, occurred more frequently in the lower lobes and were

associated with acute thromboemboli in segmental and subsegmental pulmonary arteries of the

corresponding segment. Ten (10/14, 71%) lesions displayed an ellipsoid configuration, two (2/14, 14%)

had a pyramidal shape, and two involved an almost entire pulmonary segment. The average largest

dimension was 3.9 cm (range, 2.16.7 cm). All lesions subtended one or more bronchovascular bundles;

three (3/14, 21%) showed air-bronchograms, and a thromboembolus was identified in the subtended

arteries in nine (9/14, 64%) lesions. In succeeding CT scans (eight lesions) and follow-up radiographs (three

lesions), the lesions became smaller, and the majority evolved into pleural-based linear scars by 7 months.

Conclusion: The reversed halo sign very likely corresponds to pulmonary infarction in patients with

acute PE. Its recognition may have important clinical implications.

Keywords: Pulmonary CT angiography, pulmonary embolism, reversed halo sign, pulmonary infarction

Submitted April 24, 2012; accepted for publication December 4, 2012

The reversed halo sign refers to an area of ground glass opa-

cification surrounded by a complete or almost complete rimof consolidation in computed tomographic (CT) images ofthe lungs. This unusual pattern of pulmonary opacificationwas originally described in patients with cryptogenic orga-nizing pneumonia (1, 2), and the term reversed halo wascoined by Kim et al. in 2003 (2). Later studies have shownthat the sign is also associated with other pulmonary dis-eases, including pulmonary embolism (3).

We have observed the reversed halo sign in 12 patientswith acute pulmonary embolism and infer that the sign cor-responds to pulmonary infarction based on the constellationof findings in the initial and subsequent CT examinations.These findings may be of relevance to the diagnosis of pul-

monary infarction and are described in the present paper.

Material and Methods

The reversed halo sign was an incidental observation madein 12 patients with acute PE during routine reporting ofchest CTs from June 2008 to September 2011. The CT exam-inations of the 12 patients were collected and then analyzedretrospectively. The diagnosis of pulmonary embolismwas made by CT angiography in 11 cases, and in onepatient the diagnosis was made incidentally by a routinecontrast-enhanced scan of the chest. Subsequent scans ofseven patients and follow-up chest radiographs of twopatients were also examined retrospectively. The shortestinterval between the initial and later scans was 13 days,and the longest was 2 years and 8 months. Three patients

had two or three follow-up scans which were obtained

Acta Radiologica 2013; 54: 505510. DOI: 10.1177/0284185113475797

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between 13 days and 12 months after the initial scan. Thefollow-up radiographs in the two patients were obtainedat 2 weeks and 3 months, respectively.

All studies were performed on 64-detector CT scanners(LightSpeed VCT, LightSpeed Discovery CT750 HD; GEHealthcare, Milwaukee, WI, USA). In 11 patients, a pulmon-ary embolism protocol was followed; patients received a

bolus of 55 mL of non-ionic contrast (Iohexol [Omnipaque300 mg/mL]; GE Healthcare Canada, Mississauga, ONT,Canada) followed by a 35 mL saline flush through theantecubital veins at a rate of 4.5 mL/s. The scan delay waspredetermined by a test bolus (20 mL) using the pulmonarytrunk as the region of interest. In the 12th patient, 90 mL ofnon-ionic contrast were administered intravenously at a rateof 2 mL/s, and the scan delay was 65s. Follow-up studiesincluded pulmonary CT angiograms, contrast-enhancedCT scans of the chest and in a few cases, contrast-enhancedCT scans of the abdomen, in which patients received85100 mL of non-ionic contrast intravenously at a rate of2 mL/s. The scan delay was also predetermined by a test

bolus using the liver parenchyma as the region of interest.The pulmonary CT angiograms were obtained with1.25 mm collimation at 0.9-mm intervals through thethorax; the standard studies were obtained with 5 mmcollimation at 4-mm intervals and reconstructed at 1.25 1.25 mm. The scans of the abdomen were obtained with1.25 1.25 mm collimation at 0.9-mm intervals from thebase of the lungs, above the diaphragm, to the pelvis.

The patients were between 21 and 80 years of age with amean of 49 years; seven (58%) were women. Six patients hadno significant medical history. Three patients had under-lying malignancy: metastatic adenocarcinoma of unknownprimary, invasive urinary bladder transitional cell carci-

noma, and metastatic pulmonary carcinoma. One patient,with paranoid schizophrenia and sickle cell anemia, waspositive for anti-cardiolipin antibodies and had a historyof pulmonary embolism and deep venous thrombosis(DVT). One patient had developed hypovolemic shock fol-lowing laparoscopic cholecystectomy 30 days before thepulmonary CT angiogram was performed, and anotherpatient had insulin-dependent diabetes. Six patients hadevidence of DVT at the time of their initial scans. The pre-senting symptoms are summarized in Table 1.

Results

The reversed halo sign was observed as a single lesion in10 patients; in two patients, two lesions were found. Theincidence of the sign in all patients diagnosed with pulmon-ary embolism during the collection period was not deter-mined. All lesions were pleural-based, and the majority(10/14, 71%) displayed a 3-dimensional shape resemblingan ellipsoid with its longest diameter parallel to a pleuralsurface. In cross-sectional images, these opacities appearedoval or round depending on the plane of the imagerelative to their long (or short) diameters (Figs. 1, 2a, 3).Two (2/14, 14%) lesions had a pyramidal configurationwith a broad pleural base and the apex directed towards

the hilum. These appeared as triangular or wedge-shaped

areas of central ground-glass density bordered by consoli-dation in cross-sectional images (Fig. 4). The remainingtwo lesions involved a significant portion of the inferiorsegment of the lingula (Fig. 2c) and almost the completeanterior segment of the left lower lobe, respectively. Theaverage largest dimension of the opacities was 3.9 cm(2.16.7 cm) which was always along a pleural or fissuralsurface.

All of the lesions subtended one or more peripheralbronchovascular bundles, and in 21% (3/14), the subtendedbronchi could be followed a short distance within thezones of consolidation and ground-glass density formingair-bronchograms. A thromboembolus was identified in

the subtended arteries in 64% (9/14) of the lesions(Fig. 4b); in the other cases, the vessels could not be reliablyassessed.

The lesions were located mainly in the lower lobes, occur-ring more frequently in the right lower lobe, and wereassociated with acute thromboemboli in the segmentaland subsegmental pulmonary arteries of the correspondingsegment in each case (Table 1). Except in one patient, inwhom only the left lower lobe was involved, thromboem-boli were multiple, being discovered in more proximalarteries and in the opposite lung. All of the lesions wereassociated with subtotal pulmonary embolism (i.e. obstruc-tion of the segmental and subsegmental arteries as opposed

to the lobar or main pulmonary arteries).

Table 1 Clinical features of 12 patients with pulmonary embolism

and infarction

Mean age: 49 years (range, 2180 years)

Male/Female ratio: 5/7 (n 12)

Clinical presentation (n 12)

Chest pain 6 (50%)

Shortness of breath 3 (25%)

Calf tenderness 2 (17%)

Tachycardia 1 (8%)

Syncope 1 (8%)

Past medical history (n 12)

None known 6 (50%)

Malignancy 3 (25%)

Sickle cell anemia 1 (8%)

Shock 1 (8%)

Insulin-dependent diabetes 1 (8%)

Distribution of thromboemboli (n 12)

Right main pulmonary artery 2 (17%)

Left main pulmonary artery 1 (8%)

Right upper lobe arteries 8 (67%)

Right middle lobe arteries 5 (42%)

Right lower lobe arteries 10 (83%)Left upper lobe arteries 5 (42%)

Lingular arteries 7 (58%)

Left lower lobe arteries 11 (92%)

Bilateral 9 (75%)

Site of lesion with reversed halo sign (n 14)

Right upper lobe 1 (7%)

Right lower lobe 7 (50%)

Lingula 1 (7%)

Left lower lobe 5 (36%)

Includes lobar, segmental, and subsegmental pulmonary arteries in a given

lobe

506 J Casullo and A Semionov. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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The succeeding scans of seven patients (eight lesions)and the follow-up radiographs of two others (threelesions) showed a decrease in all 11 lesions. Five of theeight lesions followed by CT had evolved into pleural-basedlinear scars between 2 and 7 months (Fig. 2e). A follow-upscan of one patient at 2 years and 8 months also showedthe formation of a linear scar (Fig. 2b), and in anotherpatient, a small focal area of scarring was present at12 months (Fig. 1d). In the remaining case, the lesionhad developed into a smaller wedge-shaped opacity at

4 months with no further follow-up.

Discussion

Kim et al. (2) observed the reversed halo sign in six of 31patients with cryptogenic organizing pneumonia and con-cluded that the sign appeared to be relatively specific forcryptogenic organizing pneumonia as they did not find asimilar pattern in any of their control cases. Previousradiologic-pathologic correlation (1) revealed that thecentral areas of ground-glass density corresponded to alveo-lar septal inflammation and cellular debris in the alveoli

with little granulation tissue, while the peripheral areas of

Fig. 1 A 51-year-old woman with metastatic adenocarcinoma of unknown primary, deep venous thrombosis and incidental bilateral pulmonary embolism. (a, b)

Transverse (a) and coronal (b) images demonstrate a 5.2-cm ellipsoid-shaped area of ground-glass density surrounded by a rim of consolidation (arrowheads) in

the anterior segment of the right lower lobe which abuts the costal, fissural (white arrows), and diaphragmatic pleural surfaces. A second lesion is present in the

adjacent lateral segment (black arrow in (a)). Note multiple subtended bronchovascular bundles at the medial margin of the lesions. (c) Transverse image of the

right lower lung from an abdominal scan obtained at 19 days shows a slight decrease in the right lower lobe lesions and almost complete replacement by soft

tissue density. There is retraction and enhancement of thickened visceral pleura (straight arrow) which adjoins a tiny loculated pleural effusion (curved arrow).

(d) Coronal image of the right lung from a routine scan of the thorax obtained at 12 months shows a small residual pleural-based opacity (arrowhead) in the

anterior segment of the right lower lobe corresponding to the previous lesion described in (a) and (b). Note the associated retraction of the adjacent lung and

major fissure (single arrow). (The double arrows indicate the minor fissure)

Reversed halo sign in acute pulmonary embolism and infarction 507. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .



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consolidation corresponded to organizing pneumonia in thealveolar ducts and adjacent alveoli.

The reversed halo sign was later described in 15 patientswith paracoccidioidomycosis (4). Surgical biopsy specimensof the lungs from three infected patients showed no evi-

dence of organizing pneumonia; the central area of thelesions was found to contain an inflammatory infiltratewithin the alveolar septa, and the periphery consisted of adense cellular infiltrate within the alveoli. The reversedhalo sign has since been observed in other pulmonary infec-tions (e.g. invasive aspergillosis, histoplasmosis, cryptoco-ccosis, pneumocystis jiroveci pneumonia, and tuberculosis),Wegener granulomatosis, sarcoidosis, bronchioloalveolarcarcinoma, and pulmonary embolism. In a recent report,seven of 79 patients with the sign were found to have pul-monary embolism; the majority had either organizing pneu-monia (18/79) or paracoccidioidomycosis (14/79) (3).

In the present study, the sign was recognized in 12

patients with acute pulmonary embolism and likely

corresponded to an area of infarction. The shape of thelesions was typically ellipsoid (10/14 or 71%) rather thantetrahedral (2/14 or 14%). From pathological observations,infarcts can assume any shape, often being irregular or geo-graphic (57). In their 1940 paper on pulmonary infarction,

Hampton and Castleman correlated postmortem findingsand the changes in antemortem and postmortem radio-graphs and noted that none of the infarcts were pyramidalin shape or truly triangular (5). In a more recent pathologi-cal study of 23 surgical specimens of pulmonary infarcts,only six (26%) were triangular or wedge-shaped (7).Furthermore, a radiologic-pathologic correlative studyof postmortem lung specimens utilizing CT found that per-ipheral wedge-shaped opacities were not specific for infarc-tion (8).

Hampton and Castleman observed that infarcts,especially those involving the costophrenic angles, pro-duced opacities with a characteristic hump-shaped

convexity directed towards the heart in radiographs of the

Fig. 2 (a, b) A 47-year-old woman with insulin-dependent diabetes, acute shortness of breath, and bilateral pulmonary embolism. The pulmonary CT angiogram

in the sagittal plane (a) demonstrates a 2.9-cm encapsulated area of ground-glass density (arrowhead) in the posterior costophrenic angle of the left lower lobe

which subtends a bronchovascular bundle (curved arrow). Note the surrounding ground-glass opacification compatible with hemorrhage. Transverse image (b) of

the left lower lobe from a CT angiogram performed at 2 years and 8 months shows the resulting linear scar (arrowhead). (c, d, e) A 67-year-old man with metastatic

bronchogenic carcinoma, acute left pleuritic chest pain, and unilateral pulmonary embolism. Transverse image (c) of the left lung from a CT angiogram demon-

strates ground-glass opacification (arrowhead) of a large portion of the inferior lingula which is encased by a thin layer of consolidation and bordered by the chest

wall, the major fissure (arrow), and the epipericardial fat (). Transverse image (d) of the left lung from a routine scan of the thorax at 15 days shows a significant

reduction in the lingular opacification (arrowhead). At 7 months, the linear scarring (arrowheads) and the pleural and fissural thickening (curved arrow) that ensued

are shown in a transverse image (e) from a routine scan of the thorax




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chest (5). In six of our patients, the lesions were nestled inthe costophrenic angles of the lower lobes and also dis-played a rounded margin facing centrally in coronal andsagittal CT images (Fig. 3; see also Figs. 1b and 2a).

Air-bronchograms were observed in three (21%) of the 14lesions, a higher frequency than previously reported (4/50)(10). In each case, one or more subtended bronchovascularbundles were seen at the medial margin of the opacities(vascular or vessel sign; (810)), and in at least 64% of thelesions, a thromboembolus was present in a subtended pul-

monary artery. Thromboemboli were also found in other

pulmonary arteries of the corresponding segment, includingthe segmental arteries.

In two CT studies on pulmonary infarcts, small lucencieswithin peripheral areas of consolidation were noted in 58%and 46% of cases, respectively (9, 10), and had a 98% speci-ficity and a 46% sensitivity for infarction (10). Histologically,the lucencies represented viable lung among necrotic sec-ondary pulmonary lobules (n 12) (9) or only coagulativenecrosis and inflammation (n 1) (10). The relativelylarger areas of central ground-glass density observed in

our cases probably reflect a similar process of coagulative

Fig. 3 (a) A 75-year-old man with no significant medical history, syncope, and bilateral pulmonary embolism. Sagittal image of the right hemithorax from a CT

angiogram demonstrates a 3.5-cm encapsulated lesion with central lucency occupying the posterior costophrenic angle of the right lower lobe. Note the upper

convex surface (curved arrow) and the bulging margins (arrowheads) outlined against a pleural effusion. (b, c) A 30-year-old woman with sickle cell anemia, acute

chest pain, and bilateral pulmonary embolism. Coronal image of the right hemithorax from a CT angiogram shows a 2.2-cm encapsulated lesion with a roundedsuperior border (arrow in (b)) nestled in the lateral costophrenic angle of the right lower lobe. The same area of opacification in a frontal radiograph obtained the

same day has a similar convex margin (arrow in (c)) directed centrally (Hamptons hump)

Fig. 4 A 29-year-old man with no significant medical history, acute deep venous thrombosis, and bilateral pulmonary embolism. (a) Transverse image of the right

upper lobe from a CT angiogram shows a 5.5-cm triangular opacity of ground-glass density and peripheral consolidation in the anterior segment. The consolida-

tion is thickest along the pleural surfaces (curved arrows). (b) In an oblique transverse reformat, the anterior segmental artery and the arterial branch supplying the

opacified area both contain thromboemboli which are separated by a tiny amount of contrast (arrow). (c) Detail of a frontal radiograph of the right upper lung

obtained at 3 months shows a small linear opacity (arrow) very likely corresponding to a residual scar in the anterior segment of the right upper lobe

Reversed halo sign in acute pulmonary embolism and infarction 509. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .



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necrosis and lobular sparing (6) in a thromboembolizedzone that still contained air.

Pulmonary infarcts heal by organization. The granulationtissue begins at the periphery and progresses centripetallyencapsulating the infarcted area (5, 7). Depending on thesize of the infarct, this process may last for weeks tomonths resulting in gradual displacement of the air and

replacement of the hemorrhagic and necrotic tissue withfibrous connective tissue. As healing continues, the infarctsbecome smaller, solidify and eventually form linear scars(5). In the seven patients with follow-up scans, shrinkagewas evident by 13 days (the shortest interval between thefirst and second scans), and residual air was present in allfour lesions that were imaged within 25 days of the initialscan. A thin pleural-based linear scar was observed asearly as 2 months, and the majority of the lesions hadevolved into linear scars by 7 months. It seems very likelythen that the peripheral consolidation in our cases corre-sponded to granulation and fibrous tissue. A componentof inflammation may have also been present at the

margins of the lesions as previously described in some sur-gical specimens (7).Pulmonary thromboembolism does not commonly result

in infarction; the incidence of infarction in autopsy subjectswith pulmonary emboli ranges from 10% to 30% (6, 11). It isbelieved that the collateral bronchial circulation and reversalof flow through the pulmonary and bronchial veins preventinfarction after pulmonary embolism in the normal lung (6).On the other hand, pulmonary venous hypertension andsystemic arterial hypotension favor the development ofinfarction (5, 6), and malignancy and hypercoagulablestates may be other contributing factors (11). Seven (58%)of our patients did not have any known predisposing con-

ditions at the time of the initial scans (which does notnecessarily imply that none existed).

In conclusion, therefore, the recognition of the reversedhalo sign in the context of acute pulmonary embolismcould raise suspicion of pulmonary infarction and mightalso have important clinical implications in those individ-uals with no known risk factors for infarction.

Conflict of interest: None.

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