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Reversed Halo: No Longer a Pathognomonic Sign
Dany Jasinowodolinski, Gustavo Meirelles, Edson Marchiori, Arthur Souza, Gilberto Szarf, Cesar De Araujo Neto, Viviane Antunes, Julia Capobianco Departments of Radiology of Fleury,
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Reversed Halo: No longer a pathognomonic sign
LEARNING OBJECTIVES To review the definition of the reversed halo sign and its association with the diagnosis of cryptogenic organizing pneumonia. To ilustrate several other abnormalities that can present the reversed halo sign. To reinforce the concept that this sign is not pathognomonic.
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REVERSED HALO SIGN DEFINITION:
The term reversed halo sign was coined by Kim et al. in 2003 to describe a central ground-glass opacity surrounded by a more dense air-space consolidation of crescentic and ring shape. At that time the authors concluded that the sign appeared relatively specific to make a diagnosis of cryptogenic organizing pneumonia on CT. Kim SJ, Lee KS, Ryu YH, Yoon YC, Choe KO, Kim TS, Sung KJ. Reversed halo sign on high-resolution CT of cryptogenic organizing pneumonia: diagnostic implications. AJR Am J Roentgenol May;180(5):
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X Reversed halo sign halo sign
The reversed halo sign is a focal rounded area of ground-glass opacity surrounded by a more or less complete ring of consolidation. The halo sign is characterized by a zone of ground-glass attenuation surrounding a pulmonary nodule or mass on CT images.
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ETIOLOGY NON-INFECTIOUS INFECTIOUS Bronchioloalveolar carcinoma
Cryptogenic organizing pneumonia Edema Eosinophilic pneumonia Pulmonary infarction Sarcoidosis Wegener’s granulomatosis ? INFECTIOUS Aspergillosis Cryptococcosis Paracoccidioidomycosis Pneumocystis jiroveci pneumonia Schistosomiasis Tuberculosis ?
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ANGIOINVASIVE PULMONARY ASPERGILLOSIS
Reversed Halo: No longer a pathognomonic sign ANGIOINVASIVE PULMONARY ASPERGILLOSIS Affects mainly neutropenic patients. Common findings: Nodules, consolidation or ground-glass opacities. Cavitation may occur. Classic signs: halo sign, air crescent sign.
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INVASIVE PULMONARY ASPERGILLOSIS
INVASIVE PULMONARY ASPERGILLOSIS B A C 44-year-old woman with chronic leukemia and fever. A. HRCT shows bilateral pleural effusion and a mass in the left lower lung, with the reversed halo sign (arrow). B. Histology demonstrates hemorrhage inside the mass. C. Grocott silver stain reveals hyphae of Aspergillus sp.
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INVASIVE PULMONARY ASPERGILLOSIS
B A C 67-year-old woman with leukemia. HRCT shows a mass in the right lower lobe, with the reversed halo sign, and ground-glass opacities in the periphery (A). Histology (Grocott silver stain) reveals hyphae of Aspergillus organisms in the periphery of the lesion, invading the pulmonary parenchyma (B), and hyphae surrounding and invading a blood vessel (C).
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PULMONARY CRYPTOCOCCOSIS
Reversed Halo: No longer a pathognomonic sign PULMONARY CRYPTOCOCCOSIS Caused by Cryptococcus neoformans which shows a worldwide distribution, especially in soil containing pigeon or avian droppings. The disease occurs predominantly in the immunocompromised patients but also occurs in immunocompetent host. HRCT - The pulmonary manifestations are variable and include masses, nodular or reticular opacities, consolidations, or miliary nodules.
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PULMONARY CRYPTOCOCCOSIS
64-year-old man with pulmonary cryptococcosis A,B. HRCT demonstrate reversed halo sign (arrow) formed by clusters of nodules in the periphery, and ground-glass opacities in the central regions. C,D. Histopathology (Mucicarmine stain) shows alveolar spaces filled with yeast (Cryptococcus neoformans).
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PULMONARY PARACOCCIDIOIDOMYCOSIS
Reversed Halo: No longer a pathognomonic sign PULMONARY PARACOCCIDIOIDOMYCOSIS The most frequent endemic systemic mycosis in Latin America caused by the fungus Paracoccidioides brasiliensis. The disease is usually asymptomatic but can progress to severe pulmonary involvement leading to progressive cough and shortness of the breath. HRCT - Ground-glass attenuation areas, small centrilobular nodules, cavitated nodules, large nodules, parenchymal bands, and areas of cicatricial emphysema.
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59-year-old man with pulmonary paracoccidioidomycosis
HRCT shows bilateral areas of reversed halo sign (arrows). Also noted are small nodules, areas of ground-glass and consolidation. A B A. Histology shows that the lesions consisted of an inflammatory infiltrate in the alveolar septa, with relative preservation of the alveolar spaces. B. Grocott-Gomori stain confirmed the presence of the fungus (P. brasiliensis).
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PNEUMOCYSTIS JIROVECI PNEUMONIA
Reversed Halo: No longer a pathognomonic sign PNEUMOCYSTIS JIROVECI PNEUMONIA pneumonia caused by a yeast-like fungal microorganism called Pneumocystis jiroveci (formerly know as Pneumocystis carinii). Commonly associated with AIDS or other immunosupression processes. HRCT: - Patchy or confluent, symmetric, bilateral ground-glass opacities and consolidation. - Interlobular septal thickening, intralobular linear opacities, cystic lesions, and nodules. - Crazy-paving pattern. - Predominate in the upper and middle lung fields.
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PNEUMOCYSTIS JIROVECI PNEUMONIA
37 year-old man with AIDS. A,B. HRCT demonstrates multiple areas of reversed halo sign (arrows)and bilateral patchy areas of ground-glass opacities. C, D Histopathology shows partial filling of air spaces by a foamy exudate, constituted mainly of surfactant, fibrin and cellular debris. E, F. The organisms are seen within this exudate in the silver stain.
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PULMONARY SCHISTOSOMIASIS
Reversed Halo: No longer a pathognomonic sign PULMONARY SCHISTOSOMIASIS Schistosomiasis is an important parasitic infection in many regions of the world, mainly in tropical areas. Three main species cause human infections (S. mansoni, S. haematobium, and S. japonicum. Humans acquire the infection following the contact with fresh water that harbours the intermediate snail host and the cercaria. Schistosomiasis is an important cause of pulmonary arterial hypertension in some countries.
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PULMONARY SCHISTOSOMIASIS
B C D A,B,C. HRCT demonstrate multiple areas of reversed halo sign in both lungs (arrows). D. Histopathology shows granulomatous inflammation, with the presence of a schistosome egg inside a granuloma.
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PULMONARY TUBERCULOSIS
Reversed Halo: No longer a pathognomonic sign PULMONARY TUBERCULOSIS Definition – Tuberculosis is na airborne infectious disease caused by Mycobacterium tuberculosis and is a major cause of morbidity and mortality, particularly in developing countries. HRCT - Post-primary tuberculosis findings include centrilobular and/or airspace nodules (tree-in-bud pattern), consolidations, cavitations, bronchial wall thickening, miliary nodules, tuberculomas, calcifications, parenchymal bands, interlobular septal thickening, ground-glass opacities, pericicatricial emphysema, and fibrotic changes.
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PULMONARY TUBERCULOSIS
32-year-old female with a 3-week history of dry cough. A.HRCT shows a nodular rim of consolidations and ground-glass denoting the reversed halo (arrows). B. HRCT obtained 3 months after treatment shows partial regression of the finding. C D C,D. Histology shows that confluent granulomas correspond to the nodular areas caracterized on CT. Figure 2B. A follow-up high-resolution CT scan obtained 3 months after the first examination, shows significant improvement of the opacities. 3 months follow-up
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BRONCHOALVEOLAR CARCINOMA
Reversed Halo: No longer a pathognomonic sign BRONCHOALVEOLAR CARCINOMA A subtype of adenocarcinoma with a pure lepidic spreading pattern and no evidence of stromal, vascular, or pleural invasion. CT patterns: Solitary nodule or mass. Diffuse nodular pattern. Focal, multifocal or diffuse areas of consolidation or ground-glass opacities, or a mixture of these patterns.
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BRONCHOALVEOLAR CARCINOMA
54-year-old man with bronchioloalveolar carcinoma. HRCT shows a small nodule in the left lower lobe with the reversed halo sign (arrow). B. Histopathology demonstrates proliferation of tumoral cells lining the alveolar wall.
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BRONCHOALVEOLAR CARCINOMA
49-year-old woman with bronchioloalveolar carcinoma . Axial (A) coronal (B) and sagital (C) images show irregular and spiculated nodule in the superior segment of left lower lobe, with the reversed halo sign. D. Histopathology shows tumoral cells filling the air space, with preservation of lung arquiteture. D
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Reversed Halo: No longer a pathognomonic sign
ORGANIZING PNEUMONIA A disease characterized by the presence of patches of granulation tissue polyps in the interior of the alveoli, alveolar ducts, and, to a lesser extent, in the bronchioles associated with focal organizing pneumonia. Can be cryptogenic (idiopathic), or secondary. The later usually related to infection, neoplasms and collagen vascular diseases. Maybe just the periphery of another lesion. HRCT: Areas of consolidation or ground-glass attenuation, typically in subpleural or peribronchial areas. - Multiple nodules, occasionally with a surrounding halo.
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CRYPTOGENIC ORGANIZING PNEUMONIA
B 62 year-old female patient with cryptogenic organizing pneumonia. A. HRCT of the lower pulmonary regions shows consolidations with the reversed halo sign in the left lower lobe (arrows). B. Histopathology demonstrate patchy involvement of the airspaces by polypoid fibroblastic foci, distributed within terminal bronchioles, alveolar ducts and alveoli (stars).
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SECONDARY ORGANIZING PNEUMONIA
B D 67 year-old man with organizing pneumonia post-chemotherapy. A,B. HRCT shows pulmonary consolidations and parenchymal bands in the right lower lobe, with the reversed halo sign (arrow). C. Histopathology demonstrate peribronchial involvement of the airspaces. D. Magnification shows a fibroblastic polyp within a alveolar space (star).
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PULMONARY EDEMA Typical findings: Ground-glass opacities.
Reversed Halo: No longer a pathognomonic sign PULMONARY EDEMA Typical findings: Ground-glass opacities. Consolidations. Peribronchovascular and interlobular septal thickening. Crazy-paving pattern. Pleural effusions.
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PULMONARY EDEMA 72 year-old patient with non-cardiogenic pulmonary edema. HRCT shows nodular ground-glass opacities surrounded by a incomplete ring of consolidation (arrows). Follow-up scan demonstrates involution of the opacities.
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CHRONIC EOSINOPHILIC PNEUMONIA
Reversed Halo: No longer a pathognomonic sign CHRONIC EOSINOPHILIC PNEUMONIA CEP is an idiopathic condition characterized by: Presence of pulmonary infiltrates on chest radiographs. Eosinophilic infiltration in lung parenchyma. Respiratory symptoms present for more than 3 weeks. Exclusion of other causes of eosinophilia. HRCT: Peripheral airspace consolidation and areas of ground-glass. predominantly in the middle or upper lung zones.
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CHRONIC EOSINOPHILIC PNEUMONIA
B A C 37 year-old female patient with chronic eosinophilic pneumonia. Chest X-ray showing peripheral pulmonary consolidations. B, C. HRCT images show peripheral reversed halo signs (arrows).
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PULMONARY INFARCTION COMMON CT FINDINGS: Peripheral consolidation
Reversed Halo: No longer a pathognomonic sign PULMONARY INFARCTION COMMON CT FINDINGS: Peripheral consolidation Ground-glass opacities Parenchymal bands Pleural effusion
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PULMONARY INFARCTION A B C
79 year-old patient with pulmonary embolism. Contrast enhanced CT shows a thrombus in the left common femoral vein (arrow in A), another thrombus in the right lower lobe artery (arrow in B) and the reversed halo sign in the right lower lobe (arrow in C). Figure 18.
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SARCOIDOSIS Granulomatous systemic disease.
Reversed Halo: No longer a pathognomonic sign SARCOIDOSIS Granulomatous systemic disease. Pulmonary involvement is common. Several radiological appearances. Typical findings: - Micronodules with perilymphatic pattern of distribution. Predominantly in upper and middle lung zones. Hilar and mediastinal lymph node enlargement.
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SARCOIDOSIS 31year woman with sarcoidosis. HRCT shows nodules and an area of reversed halo sign (arrows). Note the lobulated appearance of the consolidation, secondary to the confluent granulomas. This appearance has been previously described in the literature as the fairy ring sign and also the galaxy sarcoid sign.
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WEGENER’S GRANULOMATOSIS
Reversed Halo: No longer a pathognomonic sign WEGENER’S GRANULOMATOSIS A form of granulomatous vasculitis that manifests with the classic triad of lung disease, sinusitis accompanied by fever, and renal involvement. HRCT: Nodules or masses, ground-glass opacities or consolidations. Cavitation is common. Consolidations and ground-glass opacities are usually related with hemorrhage. Airway involvement is rare but maybe present.
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WEGENER’S GRANULOMATOSIS
52-year-old man with hemoptisis secondary to Wegener’s granulomatosis. Axial (A,B) and coronal (C) CT images demonstrate multiple pulmonary nodules with the reversed halo sign (arrow). Some nodules are cavitated. D. Histology shows necrotizing vasculitis involving a small vessel.
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IN CONCLUSION A wide spectrum of diseases can manifest the reversed halo sign on the HRCT. Although the sign is often associated with cryptogenic organizing pneumonia, it may also accompany other lesions such as inflammatory, infectious or neoplasms. Whether the reversed halo sign is a primary manifestation of the disease or a secondary organizing pneumonia associated is not always possible to be established.
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WE THINK IT HAS ALREADY LOST IT!
IN CONCLUSION “The reversed halo sign is a focal rounded area of ground-glass opacity surrounded by a more or less complete ring of consolidation. A rare sign, it was initially reported to be specific for cryptogenic organizing pneumonia but was subsequently described in patients with paracoccidioidomycosis. Similar to the halo sign, this sign will probably lose its specificity as it is recognized in other conditions” WE THINK IT HAS ALREADY LOST IT! Hansell, et al. Fleischner Society: Glossary of Terms for Thoracic Imaging. Radiology 2008; 246:
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REFERENCES Reversed Halo: No longer a pathognomonic sign
Kim SJ, et al. Reversed halo sign on high-resolution CT of cryptogenic organizing pneumonia: diagnostic implications.AJR 2003;180(5): Gasparetto EL, et al. Reversed halo sign in pulmonary paracoccidioidomycosis. AJR 2005;184(6): Bravo Soberón A, et al. High-resolution computed tomography patterns of organizing pneumonia. Arch Bronconeumol 2006;42(8):413-6. Agarwal R, et al. Another cause of reverse halo sign: Wegener's granulomatosis. Br J Radiol 2007;80(958): Benamore RE, et al. Reversed halo sign in lymphomatoid granulomatosis. Br J Radiol 2007;80(956):e162-6. Wahba H, et al. Reversed halo sign in invasive pulmonary fungal infections. Clin Infect Dis 2008;46(11): Kumazoe H, et al. "Reversed halo sign" of high-resolution computed tomography in pulmonary sarcoidosis. J Thorac Imaging 2009;24(1):66-8.
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