Swine-Origin Influenza A (H1N1) Viral Infection: Thoracic Findings on CT

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1 Cardiopulmonary Imaging Pictorial Essay Marchiori et al. CT of H1NI Viral Infection Cardiopulmonary Imaging Pictorial Essay Swine-Origin Influenza (H1N1) Viral Infection: Thoracic Findings on CT Edson Marchiori 1,2 Gláucia Zanetti 1,2 Giuseppe D Ippolito 3 Carlos Gustavo Yuji Verrastro 3 Gustavo de Souza Portes Meirelles 3 Julia Capobianco 3 Rosana Souza Rodrigues 2,4 Marchiori E, Zanetti G, D Ippolito G, et al. Keywords: CT, H1N1, pulmonary imaging, swine-origin influenza, viral infection DOI: /JR Received June 4, 2010; accepted after revision October 21, Department of Radiology, Fluminense Federal University, venue Marques do Paraná, 530 Centro, Niterói, Rio de Janeiro , razil. ddress correspondence to E. Marchiori 2 Department of Radiology, Federal University of Rio de Janeiro, Rio de Janeiro, razil. 3 Department of Radiology, Universidade Federal de São Paulo, São Paulo, razil. 4 D Or Institute for Research and Education, Rio de Janeiro, razil. CME This article is available for CME credit. See for more information. WE This is a Web exclusive article. JR 2011; 196:W723 W X/11/1966 W723 merican Roentgen Ray Society OJECTIVE. The purpose of this article is to illustrate and describe various CT manifestations of swine-origin influenza (H1N1) viral infection. CONCLUSION. The imaging findings seen in patients with H1N1 infection include consolidations, ground-glass opacities, interlobular septal thickening, small nodules, and findings suggestive of small airways disease, among others. Definitive diagnosis is based on correlation of the CT findings with the clinical symptoms and laboratory test results. I nfluenza viruses are an important cause of pandemic respiratory disease and annual seasonal influenza. Infections with the 2009 swine-origin influenza (H1N1) virus emerged in Mexico in pril 2009 and spread rapidly around the world [1, 2]. For most patients with this infection, chest radiography provides adequate imaging information. However, CT particularly high-resolution CT (HRCT) is an important tool when clinical suspicion of pneumonia is high and the radiographic findings are normal or questionable (Fig. 1). CT is also helpful in assessing complications and providing evidence of mixed pulmonary infections in patients not responding to therapy [1]. Some articles published from late 2009 and early 2010 reported on the HRCT aspects of patients with H1N1 infection. certain percentage of cases are likely to have atypical CT findings [3], so the purpose of this article is to illustrate and describe the various CT manifestations of H1N1 viral infection. ll patients included in this work fulfill the criteria established by the Centers for Disease Control and Prevention for confirmed H1N1 cases, which are influenzalike illness and positive findings for influenza (H1N1) virus on reverse transcriptase polymerase chain reaction or viral culture assays [1 3]. Cases of H1N1 with superimposed bacterial pneumonia were excluded using clinical and laboratory criteria. Clinical and Laboratory Findings The most common clinical findings for H1N1 virus infection at presentation are fe- ver, cough, dyspnea, myalgia, and headache. Most cases are mild and self-limited; however, a small percentage of individuals have a severe course that may result in respiratory failure and death [4 6]. severe course and fatal outcome are more frequent in individuals with concomitant chronic diseases but also can occur in previously healthy people [3, 6]. Pathologic Findings The most frequent pathologic findings include classic exudative diffuse alveolar damage with alveolar and interstitial edema, alveolar fibrinous exudate with hyaline membranes and reactive pneumocytes; severe necrotizing bronchiolitis characterized by extensive necrosis of the bronchiolar wall and dense neutrophilic infiltrate within the bronchiolar lumen; and exudative diffuse alveolar damage with an intense hemorrhagic component. Patients also may develop thrombosis of the pulmonary arteries. In the latter stages, fibrosing and organizing diffuse alveolar damage may be seen [6, 7]. CT Parenchymal Findings The predominant CT findings in patients with H1N1 infection are ground-glass opacities, areas of consolidation, or a mixed pattern of ground-glass opacities and areas of consolidation [1, 3, 5, 8]. The abnormalities are frequently bilateral and may have a peripheral subpleural [1, 3, 5] (Fig. 2), peribronchovascular [3, 5] (Figs. 3 and 4), lobular (Fig. 5), or random distribution [1]. Parenchymal abnormalities also may be diffuse without zonal predominance [8] or, more rarely, unilateral [5] JR:196, June 2011 W723

2 Marchiori et al. (Fig. 6). Patients with widespread consolidations have a more severe clinical course than those who do not [1] (Fig. 7). lthough none of these patterns is specific of H1N1 infection, the main patterns of disease that are most suggestive of H1N1 are scattered lung consolidations, ground-glass opacities, or both in a peribronchovascular or subpleural distribution. lthough the presence of areas of consolidation with lobar distribution on HRCT is somewhat different from the typical pattern seen in viral pneumonia and may be consistent with secondary bacterial pneumonia [2, 4], this appearance may be seen in patients with influenza (H1N1) viral infection without secondary bacterial infection [3] (Fig. 8). In these cases, a differential diagnosis should be based on clinical and laboratory findings. Scattered interlobular septal thickening associated with ground-glass opacities has been reported in some cases [4, 8] (Fig. 9); however, a crazy paving pattern has not been reported previously but is shown here (Fig. 10). nother uncommon parenchymal finding is the halo sign, which is ground-glass opacities surrounding a consolidation, nodule, or mass [3] (Fig. 11). lthough most reports do not describe findings of small airways disease as being commonly associated with viral pulmonary infection [9], Elicker et al. [3] reported that CT features associated with either large or small airways disease such as airway thickening or dilatation, centrilobular nodules (Fig. 12), and tree-in-bud opacities were frequent in their series of immunocompromised patients. The imaging appearance of H1N1 infection may be determined by the duration of illness and the patient s underlying health. Little information is available in the literature regarding CT during the recovery period of H1N1 infection. Often, multifocal areas of consolidation develop during follow-up of patients with H1N1 infection. In this situation, the differential diagnosis with secondary bacterial infection is very difficult. However, in most cases, the pulmonary opacities secondary to H1N1 infection regress during convalescence. Even in H1N1 cases with benign evolution, the consolidations may occasionally progress to linear opacities (parenchymal bands), which probably represent organizing pneumonia [10] (Figs. 13 and 14), or air trapping may develop (Fig. 15), which is clinically and radiologically suggestive of bronchiolitis. The CT abnormalities seen in cases of H1N1 infection in immunocompromised patients seem less severe than those seen in immunocompetent patients. It is possible that immunocompromised patients, at least initially, do not develop the same inflammatory response to infection as immunocompetent patients, resulting in less extensive diffuse alveolar damage. Small airways involvement manifested as centrilobular nodules and tree-in-bud opacities was the most frequent finding in the immunocompromised population described by Elicker et al. [3]. These small airways findings were distinctly absent in other series of H1N1 cases in immunocompetent patients. These small airways abnormalities may possibly become obscured later in the disease process when more extensive diffuse alveolar damage is present [3]. Extraparenchymal Findings Pulmonary emboli located on the main, lobar, segmental, and subsegmental pulmonary arteries were identified by garwal et al. [8] on contrast-enhanced CT of patients with H1N1 infection. Some patients had deep venous thrombosis in the leg veins seen on indirect CT venography and confirmed by ultrasound [8]. Parenchymal damage may predispose individuals who become infected with H1N1 virus to the formation of cysts that may rupture, causing the formation of an extraalveolar air collection. The free air may dissect and rupture through the visceral pleura, causing pneumothorax, or may track centrally into the hila and mediastinum, causing pneumomediastinum [3, 7] (Fig. 16). Small unilateral pleural effusion or bilateral pleural effusions have been reported [1, 11, 12]. However, in most studies, chest CT with soft-tissue window settings displayed several notable negative findings including the absence of lymphadenopathy [1, 3, 5, 11] and pleural or pericardial effusions [11]. Differential Diagnosis Radiologic findings of peripheral scattered areas of consolidation or ground-glass opacities are not specific for influenza pneumonia. The radiologic differential diagnosis for the most common form of H1N1 presentation that is, subpleural or peribronchovascular ground-glass opacities or consolidations is made especially with cryptogenic organizing pneumonia (COP) and chronic eosinophilic pneumonia (CEP). Imaging findings are most useful in the context of clinical symptoms, contact history, and laboratory results [7]. Sudden onset of infectious symptoms in H1N1 pneumonia is the main parameter for differentiating H1N1 infection from COP and CEP. The diseases most likely to be confused with H1N1 infection on the basis of clinical findings are other bacterial, atypical, fungal, and viral infections. Clinical and laboratory data and the presence of unusual imaging findings seen in H1N1 infection, such as pleural effusion, lymphadenopathy, and lobar consolidation, can help in establishing the correct diagnosis [13]. lthough the CT findings of H1N1 infection frequently overlap with those of other infections, a pattern of extensive or diffuse ground-glass opacities and consolidations, mainly when in a peribronchovascular or subpleural distribution, can be highly correlated to H1N1 infection [5]. Less typical tomographic presentations have a broad differential diagnosis. specific discussion of each of these patterns and their causes is beyond the scope of this work. The finding of ground-glass opacities on HRCT in patients with IDS is highly related to Pneumocystis jiroveci pneumonia. H1N1 infection should also be included in the differential diagnosis of pulmonary infections that cause ground-glass opacities in patients with IDS [14]. In these patients, measurement of the lactate dehydrogenase level is not helpful for the differential diagnosis because the lactate dehydrogenase level can be raised by either disease. Less often, other diseases in patients with IDS such as cytomegalovirus pneumonia, lymphocytic interstitial pneumonia, and nonspecific interstitial pneumonia may present as groundglass opacities on HRCT [15]. Viral infections have a broad spectrum of CT findings that include consolidation, ground-glass opacities, interlobular septal thickening, centrilobular nodules, airway thickening, and air trapping or mosaic perfusion. These findings often overlap with those of bacterial, fungal, or mycobacterial infection. Thus, imaging findings are often nonspecific for an infection agent [3]. Conclusion Pulmonary H1N1 infection can present with a wide variety of CT patterns, none of which is specific for the diagnosis. However, when associated with clinical and laboratory data, imaging findings can be of great value in staging disease, assessing complications, and following up patients, especially in cases with a severe course. References 1. Marchiori E, Zanetti G, Hochhegger, et al. Highresolution computed tomography findings from W724 JR:196, June 2011

3 CT of H1NI Viral Infection adult patients with influenza (H1N1) virus-associated pneumonia. Eur J Radiol 2010; 74: Gill JR, Sheng ZM, Ely SF, et al. Pulmonary pathologic findings of fatal 2009 pandemic influenza /H1N1 viral infections. rch Pathol Lab Med 2010; 134: Elicker M, Schwartz S, Liu C, et al. Thoracic CT findings of novel influenza (H1N1) infection in immunocompromised patients. Emerg Radiol 2010; 17: Lee CW, Seo J, Song JW, et al. Pulmonary complication of novel influenza (H1N1) infection: imaging features in two patients. Korean J Radiol 2009; 10: jlan M, Quiney, Nicolaou S, Müller NL. Swine-origin influenza (H1N1) viral infection: radiographic and CT findings. JR 2009; 193: Mauad T, Hajjar L, Callegari GD, et al. Lung pathology in fatal novel human influenza (H1N1) infection. m J Respir Crit Care Med 2010; 181: Guo HH, Sweeney RT, Regula D, Leung N. est cases from the FIP: fatal 2009 influenza (H1N1) infection, complicated by acute respiratory distress syndrome and pulmonary interstitial emphysema. RadioGraphics 2010; 30: garwal PP, Cinti S, Kazerooni E. Chest radiographic and CT findings in novel swine-origin influenza (H1N1) virus (S-OIV) infection. JR 2009; 193: Ketai LH. Conventional wisdom: unconventional virus. JR 2009; 193: Marchiori E, Zanetti G, Mano CM, Hochhegger, Irion KL. Follow-up aspects of influenza (H1N1) virus-associated pneumonia: the role of high-resolution computed tomography in the evaluation of the recovery phase. Korean J Radiol 2010; 11: Mollura DJ, snis DS, Crupi RS, et al. Imaging findings in a fatal case of pandemic swine-origin influenza (H1N1). JR 2009; 193: Marchiori E, Zanetti G, Hochhegger, Mano CM. High-resolution computed tomography findings in a patient with influenza (H1N1) virus-associated pneumonia. r J Radiol 2010; 83: viram G, ar-shai, Sosna J, et al. H1N1 influenza: initial chest radiographic findings in helping predict patient outcome. Radiology 2010; 255: Marchiori E, Zanetti G, Hochhegger, Iron KL. High-resolution computed tomography findings in a patient HIV-positive with swine-origin influenza (H1N1) virus-associated pneumonia. r J Radiol 2010; 83: Marchiori E, Müller NL, Soares Souza Jr, Escuissato DL, Gasparetto EL, Franquet T. Pulmonary disease in patients with IDS: high-resolution CT and pathologic findings. JR 2005; 184: Fig year-old man with H1N1 pneumonia., Chest radiograph shows normal lungs., CT image obtained on same day as shows mild ground-glass opacity in both lungs that predominates in lower lobes. Fig year-old man with H1N1 pneumonia. and, CT image () and reconstruction () show bilateral and predominantly peripheral focal ground-glass opacities in both lungs. Fig year-old woman with H1N1 pneumonia. CT image shows consolidations with peribronchovascular distribution in right lung base. Left lung is normal. JR:196, June 2011 W725

4 Marchiori et al. Fig year-old man with H1N1 pneumonia. and, CT images at carina level () and main bronchi level () show bilateral round consolidations with peribronchovascular distribution. lso seen is small bilateral pleural effusion (arrowheads). Fig year-old woman with H1N1 pneumonia. C, xial CT image (), coronal reformatted image (), and sagittal reformatted image (C) show bilateral patchy areas of ground-glass opacity (arrows, C) predominating in upper lobes in lobular pattern. C Fig year-old man with H1N1 pneumonia. CT image shows extensive ground-glass opacity in left upper lobe with air bronchograms. Fig year-old woman with H1N1 pneumonia., CT image shows bilateral consolidations (arrowheads) predominantly involving upper lung regions., Coronal reconstruction shows that consolidations are diffuse but predominate in upper lung portions. lso seen is bilateral pleural effusion. W726 JR:196, June 2011

5 CT of H1NI Viral Infection Fig year-old man with H1N1 pneumonia., xial CT image of right lung shows smooth septal thickening in middle lobe (arrowheads)., xial CT image of lower lobes shows crazy paving pattern (arrows) in middle lobe, consolidations in right lower lobe, and ground-glass opacity on left side. Fig. 8 4-year-old immunocompetent girl with H1N1 pneumonia. CT image shows consolidation with air bronchograms and ground-glass opacity in middle lobe. Fig year-old man with H1N1 pneumonia. CT image obtained at level of upper lobes shows patchy areas of groundglass opacity with smooth septal thickening (crazy paving pattern). lso note bilateral posterior consolidations in upper lobes. Fig year-old immunocompetent woman with H1N1 pneumonia. CT image obtained at level of lower lobes shows round mass in right lower lobe with discrete ground-glass halo (halo sign). Fig year-old male immunocompetent patient with H1N1 pneumonia. and, Coronal () and sagittal () CT reconstructions show multiple small centrilobular lung nodules, mainly in middle and right lower lobe, with areas of confluence and branching structures (tree-in-bud pattern); these findings are consistent with peripheral airway disease. JR:196, June 2011 W727

6 Marchiori et al. Fig year-old woman with H1N1 pneumonia. CT image obtained 1 month after onset of symptoms shows bilateral linear opacities (parenchymal bands) in lower lobes. Fig year-old woman with H1N1 pneumonia. CT image obtained 2 weeks after onset of symptoms shows consolidations and perilobular thickening in both lower lobes consistent with organizing pneumonia. Fig year-old woman with H1N1 pneumonia., End-inspiration high-resolution CT image obtained 2 months after onset of symptoms shows very subtle mosaic attenuation pattern in left lower lobe., Full-expiration scan obtained at same level as highlights irregular area of air trapping in left lower lobe. Fig year-old woman with H1N1 pneumonia. and, xial CT images (lung window setting) show bilateral patchy areas of consolidation and ground-glass opacity. Pneumomediastinum, small pneumothorax (arrow, ), and subcutaneous emphysema are also seen. FOR YOUR INFORMTION This article is available for CME credit. See for more information. W728 JR:196, June 2011

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