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1 Department of Diagnostic Radiology, University of Paraná, Curitiba,
Brazil.
2 University of Campinas, Campinas, Brazil.
3 Faculdade de Medicina de São José do Rio Preto, São
José Rio Preto, Brazil.
4 University of Rio de Janeiro, Rio de Janeiro, Brazil.
5 Department of Radiology, Vancouver General Hospital, 899 W 12th Ave.,
Vancouver, BC V5Z 1M9, Canada.
Received July 16, 2004;
accepted after revision August 19, 2004.
Address correspondence to N. L. Müller.
Abstract
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MATERIALS AND METHODS. The high-resolution CT scans (1- or 2- mm collimation scans) of 148 consecutive patients with proven pulmonary paracoccidioidomycosis were reviewed to determine the prevalence of the reversed halo sign in these patients. The reversed halo sign was defined as central ground-glass opacity surrounded by a crescent or ring of consolidation. The images were reviewed by two radiologists who reached a decision by consensus.
RESULTS. A reversed halo sign was found in 15 patients (10%), including 13 men and two women ranging in age from 20 to 58 years (mean, 48 years). Three patients had only one reversed halo sign, one had two lesions, and the remaining had multiple lesions. The size of the sign ranged from 10 to 50 mm (average, 20 mm). In two cases the reversed halo sign was the only finding on CT. The most common associated findings seen in the remaining 13 patients included bilateral patchy areas of ground-glass attenuation (n = 10), parenchymal bands (n = 8), and small centrilobular nodules (n = 8). Three patients underwent surgical lung biopsy. Histologically the central area of the lesions consisted of an inflammatory infiltrate in the alveolar septa, composed of macrophages, lymphocytes, plasma cells, and some giant cells, with relative preservation of the alveolar spaces. The periphery of the lesion consisted of dense and homogeneous intraalveolar cellular infiltrate. There was no evidence of organizing pneumonia.
CONCLUSION. The reversed halo sign is seen in approximately 10% of patients with paracoccidioidomycosis. In these patients, this sign reflects the presence of a central area of predominantly interstitial inflammation surrounded by predominantly air-space infiltration.
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Although paracoccidioidomycosis is a common cause of pulmonary complications in Latin America, there are only a few reports of the high-resolution CT findings associated with this entity. The most commonly described abnormalities are interlobular septal thickening and ground-glass opacities [4-6].
The reversed halo sign refers to a high-resolution CT finding that consists of a focal round area of ground-glass attenuation surrounded by a crescent or ring of consolidation [7, 8]. This sign was first presented by Voloudaki et al. [7], and it was then studied by Kim et al. [8] who found it to be relatively specific for cryptogenic organizing pneumonia.
The purpose of this study was to evaluate the prevalence of the reversed halo sign in pulmonary paracoccidioidomycosis and to assess the presence of associated findings.
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Three patients underwent surgical lung biopsy and histopathologic examination of at least one reversed halo sign lesion. In these patients, the pathologic findings were compared with the CT findings.
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The number of reversed halo signs seen in the 15 patients varied from one to more than 10. Three patients had only one sign, one had two lesions, and the remaining had multiple lesions. The size of the sign ranged from 10 to 50 mm (average, 20 mm). The reversed halo sign was identified in the upper lung zones (n = 4), middle lung zones (n = 13), and lower lung zones (n = 10). The lesions were present predominately in the periphery of the lungs in 13 cases and predominately in the central areas in two patients.
In the three patients who underwent surgical lung biopsy, histologically the central area of the lesions consisted of an inflammatory infiltrate in the alveolar septa, composed of macrophages, lymphocytes, plasma cells, and some giant cells, with relative preservation of the alveolar spaces. The periphery of the lesion consisted of dense and homogeneous intraalveolar cellular infiltrate. There was no evidence of organizing pneumonia. Grocott-Gomori methenamine-silver stain confirmed the presence of the fungus (P. brasiliensis) in the alveolar septa and in the air spaces.
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The disease is acquired by inhalation of infective particles that reach the lungs and initiate the primary infection [2]. The initial lesion is similar to the primary complex of tuberculosis and is controlled by natural defensive mechanisms or progresses to symptomatic disease [4]. Two main clinical forms of the disease are recognized: an acute form and a localized or multifocal chronic form. The acute form occurs most commonly in young male and female patients and involves mainly the reticuloendothelial system, whereas the chronic form is most prevalent in adult men and has a predominant pulmonary and mucocutaneous distribution [1].
Despite the epidemiologic importance of paracoccidioidomycosis in Latin America, only a few studies have assessed the thoracic high-resolution CT manifestations. Muniz et al. [4] reviewed the high-resolution CT findings of 30 patients with pulmonary paracoccidioidomycosis. The most frequent findings consisted of interlobular septal thickening, ground-glass opacities, nodular opacities, irregular air-space enlargement, and bronchial wall thickening. Funari et al. [6], reviewed the high-resolution CT findings in 38 patients with paracoccidioidomycosis. The main findings were interlobular septal thickening, nodular opacities, traction bronchiectasis, peribronchovascular interstitial thickening, and paracicatricial emphysema. Neither of these two studies mentioned any findings that could be interpreted as a reversed halo sign. However, in the current study, a reversed halo sign was seen in 10% of patients with paracoccidioidomycosis. Other common findings on high-resolution CT in our study were ground-glass opacities, parenchymal bands, small centrilobular nodules, and cavitated nodules.
In 1996, Voloudaki et al. [7] reported two cases of cryptogenic organizing pneumonia that manifested on high-resolution CT as central ground-glass opacity surrounded by denser air-space consolidation of crescent and ring shapes. In their study, the central ground-glass opacity corresponded histologically to alveolar septal inflammation and cellular debris, and the ring-shaped or crescentic peripheral air-space consolidation, to areas of organizing pneumonia within the alveolar ducts.
In 2003, Kim et al. [8] reviewed the high-resolution CT findings of 31 patients with cryptogenic organizing pneumonia. In six of the 31 patients they identified a central ground-glass opacity surrounded by denser consolidation of crescent or ring shape, similar to the finding described by Voloudaki et al. [7]. Kim et al. named this finding the "reversed halo sign." The sign was seen only in patients with cryptogenic organizing pneumonia and was not seen in any of the other patients: 14 patients with Wegener's granulomatosis, 10 with diffuse bronchioloalveolar carcinoma, and five with chronic eosinophilic pneumonia. They concluded that the finding therefore was highly suggestive of cryptogenic organizing pneumonia.
We observed the reversed halo sign in 15 patients with paracoccidioidomycosis. Surgical lung biopsy specimens in three of these patients showed that the central areas, corresponding to the areas of ground-glass attenuation on CT, consisted of an inflammatory infiltrate involving mainly the alveolar septa. The peripheral regions, corresponding to the consolidation on CT, consisted of dense and homogeneous intraalveolar inflammatory infiltrates. These findings indicate that the reversed halo sign can be seen in patients with active infection and is therefore not specific for cryptogenic organizing pneumonia.
In conclusion, our study shows that the reversed halo sign can be seen in patients with active infection and without organizing pneumonia. The finding is seen in 10% of patients with active P. braziliensis infection. Histologic examination revealed that the areas of ground-glass attenuation corresponded to inflammatory infiltrates in the alveolar septa and the peripheral consolidation reflected the presence of areas of intraalveolar inflammatory infiltrates without organizing pneumonia.
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