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Document downloaded from http://www.archbronconeumol.org, day 15/12/2014. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
The Halo Sign in Computed Tomography Images: Differential
Diagnosis and Correlation With Pathology Findings

Manuel Parrón,a Isabel Torres,a Mercedes Pardo,a Carmen Morales,b Marta Navarro,band Marta Martínez-Schmizcrafta aServicio de Radiodiagnóstico, Hospital Universitario La Paz, Madrid, SpainbDepartamento de Anatomía Patológica, Hospital Universitario La Paz, Madrid, Spain The halo sign is a circular area of ground-glass
Signo del halo en la tomografía computarizada attenuation that is seen around pulmonary nodules at
de tórax: diagnóstico diferencial con correlación computed tomography (CT). Although the sign is most often
an indication of pulmonary hemorrhage, it may also
accompany other lesions associated with different disease

El signo del halo consiste en un área circular de atenua-
processes. Examples are hemorrhagic nodules of infectious
ción en vidrio deslustrado que rodea un nódulo pulmonar.
origin (mucormycosis, candidiasis, tuberculosis, viral
Aunque la causa más frecuente es la hemorragia pulmonar,
pneumonia, and invasive aspergillosis—the last being the
dicho signo se asocia a numerosas entidades, que correspon-
most common cause of the CT halo sign); hemorrhagic
den a diferentes procesos anatomopatológicos: nódulos
nodules of noninfectious origin (Wegener granulomatosis,
hemorrágicos de etiología infecciosa (aspergilosis invasiva
Kaposi sarcoma, and hemorrhagic metastases); tumor
—la causa más frecuente de nódulos pulmonares con halo—,
cell infiltration (bronchioloalveolar carcinoma, lymphoma,
mucormicosis, candidiasis, tuberculosis, neumonías víricas),
and metastasis with intra-alveolar tumor growth); and
nódulos hemorrágicos de etiología no infecciosa (granulo-
nonhemorrhagic lesions (sarcoidosis and organizing
matosis de Wegener, sarcoma de Kaposi, metástasis hemo-
pneumonia). Diagnosis must therefore be based on careful
rrágicas), nódulos con halo debido a infiltración de células
consideration of all the CT chest findings within the context
neoplásicas (carcinoma bronquioloalveolar, linfoma, metás-
of the patient's clinical state. The aim of this review was to
tasis con crecimiento tumoral intraalveolar) y nódulos con
describe and illustrate different disease processes that
halo debido a lesiones inflamatorias no hemorrágicas (sar-
appear as a halo sign on CT scans, to analyze the value of
coidosis, neumonía organizada). Por lo tanto, el diagnóstico
this diagnostic tool, and to assess its correlation with
debe realizarse integrando todos los hallazgos de la tomo-
grafía computarizada de tórax en el contexto clínico del pa-
ciente. El objetivo de la presente revisión es describir e ilus-
trar enfermedades que pueden manifestarse como nódulos
pulmonares con el signo del halo, analizando su utilidad
diagnóstica y discutiendo su correlación radiopatológica.

Key words: Lung. Computed tomography. CT. Lung Infection.
Palabras clave: Pulmón. Tomografía computarizada. Infección
Lung tumors. Pulmonary nodule. Aspergillosis. Image findings. pulmonar. Neoplasia pulmonar. Nódulo pulmonar. Aspergilosis.
Signos en imagen.
mechanisms that can cause a pulmonary nodule tohemorrhage vary according to the underlying disease The chest computed tomography (CT) halo sign is an process, but they are associated with vasculitis, neovascular area of ground-glass attenuation seen around a pulmonary tissue fragility, hemorrhagic pulmonary infarction, necrosis, nodule or mass with central soft-tissue attenuation. The bronchoarterial fistula, and even transbronchial biopsy sign was first described by Kuhlman et al1 in patients with injury.2-4 The halo sign has also been linked to a wide hemorrhagic nodules associated with invasive pulmonary variety of other anatomical and disease processes, however, aspergillosis. Following this description, it was initially though such associations are less common. One example believed that the halo sign always indicated the presence is nonhemorrhagic infiltration by tumor or inflammatory of hemorrhagic pulmonary nodules.2 The pathophysiologic The aim of this review was to describe and illustrate Correspondence: Dr M. Parrón different disease processes that can manifest with a halo Servicio de Radiodiagnóstico, Hospital Universitario La Paz sign on chest CT scans, to analyze the diagnostic value of P.º de la Castellana, 261, 28046 Madrid, SpainE-mail: mppajares@hotmail.com this sign, and to assess its correlation with pathologyfindings in order to further our understanding of this Manuscript received September 5, 2007. Accepted for publication October 16,2007.
diagnostic tool. Arch Bronconeumol. 2008;44(7):386-92 Document downloaded from http://www.archbronconeumol.org, day 15/12/2014. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
PARRÓN M ET AL. THE HALO SIGN IN COMPUTED TOMOGRAPHY IMAGES: DIFFERENTIAL DIAGNOSIS AND CORRELATION WITH PATHOLOGY FINDINGS Figure 1. Invasive pulmonary aspergillosis. A: Computed tomography (CT) scan of a patient with acute lymphoid leukemia and neutropenia showing a
nodule surrounded by a halo in the right upper lobe, with adjacent acinar involvement (arrows). In the follow-up CT scan (not shown) taken after 3 weeks
of treatment with amphotericin B, the nodule had cavitated but the halo sign was no longer visible. B: Macroscopic sagittal slice of another patient's lung
showing a round necrotic lesion (asterisk) surrounded by a hemorrhagic halo (arrowheads), corresponding to invasive pulmonary aspergillosis
. C: Microscopic
image of the margin of the lesion described in B, with visible pulmonary necrosis and hemorrhage. The image also shows the hyphae of Aspergillus fumigatus
(arrows), which are of regular caliber, septate, and branching at acute angles (hematoxylin-eosin, magnification ×2).
distinctive acute-angle branching. The halo around thenodule corresponds to hemorrhagic necrosis2,9,10 (Figures When the halo sign is detected in immunocompromised patients, it is most often an indication of infectious diseaseand, in most cases, the sign corresponds to hemorrhagic Other fungi. The lung may also become infected by other fungi, such as Mucor species, which cause often-fatal opportunistic infections in patients with diabetes or a compromised immune system. Characteristic radiologicfindings include single or multiple nodules and areas of Aspergillosis. The halo sign was first described in patients consolidation that may extend to more than a single lobe.
with acute leukemia and invasive pulmonaryaspergillosis1—the latter being the most common causeof the CT halo sign in immunocompromised patients.5 Causes of Pulmonary Nodules With a Halo Sign
Pulmonary aspergillosis belongs to a clinical spectrum ofdiseases caused by the fungus Aspergillus fumigatus. It Fungi: invasive aspergillosis; infection by Mucor, Candida, can take many forms, including aspergilloma, allergic Cryptococcus, and Coccidioides species bronchopulmonary aspergillosis, chronic necrotizing Viruses: herpes simplex virus, cytomegalovirus, aspergillosis, airway-invasive aspergillosis, and invasive varicella-zoster virus, myxovirus pulmonary aspergillosis. Invasive pulmonary aspergillosis Bacteria: slow-resolving bacterial pneumonia, Coxiella affects immunosuppressed patients, and particularly those burnetii, Actinomyces species Mycobacteria: Mycobacterium tuberculosis, Mycobacterium with marked neutropenia. Its clinical manifestations are quite nonspecific and include cough, chest pain, and Parasites: Paragonimus and Schistosoma species hemoptysis. Fungal infections must therefore be considered in the differential diagnosis of a severely immunocompromised patient with fever, and because invasive pulmonary aspergillosis is associated with high mortality, it is very Hemorrhagic metastasis of angiosarcoma, choriocarcinoma, melanoma, osteosarcoma, and renal cell carcinoma important to reach a quick diagnosis and initiate aggressive Nonhemorrhagic metastases of adenocarcinoma of the treatment immediately. Although invasive pulmonary digestive tube, pancreas, and lung aspergillosis has several characteristic CT findings, such as cavitation and the air crescent sign, these only become Primary angiosarcoma evident late in the course of infection.6,7 The halo sign, incontrast, appears in the early stages of disease, and in the Noninfectious inflammatory diseases Wegener granulomatosis right clinical setting, it can be useful in the early diagnosis of aspergillosis1,8 (Figure 1A). Organizing pneumonia The invasion of small and medium-sized lung vessels Eosinophilic diseases by A fumigatus causes thrombosis and hemorrhagic infarction. In such cases, the central nodule on the CT EndometriosisTransbronchial biopsy injury (in lung transplant patients) scan corresponds to a central area of necrosis and the fungal hyphae—which are morphologically characteristic in that they are septate, and have a regular diameter and Arch Bronconeumol. 2008;44(7):386-92 Document downloaded from http://www.archbronconeumol.org, day 15/12/2014. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
PARRÓN M ET AL. THE HALO SIGN IN COMPUTED TOMOGRAPHY IMAGES: DIFFERENTIAL DIAGNOSIS AND CORRELATION WITH PATHOLOGY FINDINGS Figure 2. Hemorrhagic metastasis in a patient with choriocarcinoma who presented with massive hemoptysis. A: Computed tomography scan of the chest
shows multiple hemorrhagic pulmonary nodules with a halo sign that have coalesced in the posterior segments of the right lung. B: Macroscopic lung slice
showing several round hemorrhagic lesions. C: Macroscopic image of nodules containing hemorrhagic areas, fibrin, and tumor cells (hematoxylin-eosin,
magnification
×10).
Pathology typically shows the characteristic angioinvasion by the variable-caliber, aseptate, and right-angle branchinghyphae of these species. CT findings then show pulmonary A halo around a tumor nodule in the lung may be due nodules with a halo sign corresponding to thrombosis and to hemorrhage from the nodule itself or to the infiltration hemorrhagic pulmonary infarction when the infection of tumor cells into the adjacent lung parenchyma. invades the lung.10,11 Lung infection due to Candida species may also manifest Hemorrhagic Tumor Nodules with a halo sign on a CT scan.2,8 Pulmonary candidiasisacquired by hematogenous dissemination, for example, A variety of lung tumor processes can cause causes microabscesses, vasculitis, infected thrombi, and hemorrhaging that appears as a halo around a pulmonary areas of hemorrhagic infarction.3 nodule on the CT chest scan. Such tumors are Infections due to Cryptococcus and Coccidioides species hypervascular, with fragile neovascular tissue whose rupture may also, exceptionally, manifest with a halo sign.2,8,12 causes pulmonary bleeding.2 Examples include metastatictumors in angiosarcoma, choriocarcinoma, melanoma,osteosarcoma, and renal cell carcinoma.2,3,14,20,21 Choriocarcinoma tumor cells, for example, have a Viral pneumonia occurs more frequently in characteristic ability to erode blood vessels, causing immunocompromised patients, for whom prognosis is also bleeding3 (Figure 2). poorer. CT findings are variable and include centrilobular Several primary lung tumors, including pulmonary nodules, segmental areas of consolidation, areas of ground- angiosarcoma and Kaposi sarcoma, can also form glass attenuation with or without interlobular septal thickening, hemorrhagic pulmonary nodules.2,22 Primary Kaposi and pulmonary nodules.13 Many viruses can cause lung sarcoma is most common in homosexual males with human infection but those that are most frequently associated with immunodeficiency virus infection, and both immunologic the CT halo sign are herpes simplex viruses, cytomegalovirus, and infectious factors (such as coinfection by herpes varicella-zoster virus, and myxovirus2,8,14 On histopathologic simplex virus type 8) are thought to be implicated in the examination, the halo sign in viral pneumonia generally mechanisms of disease. CT findings for such patients corresponds to intra-alveolar hemorrhage.13 generally reveal poorly defined, peribronchovascular nodules that are occasionallysurrounded by a halo.5 Histologic features include thin- walled vascular spaces and red blood cells extravasated Mycobacterium tuberculosis and Mycobacterium avium due to wall rupture. These blood cells appear as a halo on intracellulare infections have also been reported to cause an area of ground-glass attenuation around pulmonarynodules in CT images.14-17 The origin of the halo sign in Tumor Cell Infiltration this case is not clear as it may be due to either alveolarhemorrhage or a granulomatous reaction without A halo around a tumor nodule may also indicate tumor cell infiltration. There are 2 basic forms of tumor growth Other infectious diseases that can exceptionally manifest in the lung: the first, and most common, involves the with a CT halo sign are Coxiella burnetii infection, parasitic proliferation of infiltrating tumor cells that destroy lung disease such as paragonimiasis and schistosomiasis, slow- tissue (expansive growth), while the second respects the resolution bacterial pneumonia, septic emboli, and pulmonary architecture, as tumor cells spread by attaching actinomycosis.3,18,19 In such cases, the halo sign is caused to the alveolar walls (intra-alveolar or lepidic growth).
by the infiltration of inflammatory cells and exudates into This latter form of growth is mostly associated with bronchioloalveolar carcinoma and exceptionally with Arch Bronconeumol. 2008;44(7):386-92 Document downloaded from http://www.archbronconeumol.org, day 15/12/2014. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
PARRÓN M ET AL. THE HALO SIGN IN COMPUTED TOMOGRAPHY IMAGES: DIFFERENTIAL DIAGNOSIS AND CORRELATION WITH PATHOLOGY FINDINGS Figure 3. Bronchioloalveolar carcinoma
in a patient with chronic cough. A:
Computed tomography scan of the
chest shows nodules with a halo sign
in the right lung, with some
pseudocavitation (arrow). Also visible
is a considerable area of consolidation
in the left lung. B: Microscopic image
showing thickened alveolar walls
(asterisks) due to infiltration by tumor
cells (arrows) (hematoxylin-eosin,
magnification
×10).
metastatic adenocarcinoma of the digestive tube, pancreas, lymphoid tissue lymphomas), secondary lymphomas, and or lung.24-26 The halo sign in these cases corresponds to posttransplant lymphoproliferative disease.32-34 The nodule alveolar wall thickening due to the spread of tumor cells, seen in such cases corresponds to the dense central tumor with partial occupation of the alveolar air space.2,23 infiltration area while the halo corresponds to the less dense Quantifying the size of the halo sign in small peripheral interstitial tumor cells around the nodule14,33 (Figure 4). lung adenocarcinomas may be of prognostic value asseveral authors have reported that the larger the halo sign, Noninfectious and Nontumoral Diseases
the greater the bronchioloalveolar carcinoma componentand, consequently, the better the prognosis.27-29 The diseases described in this section can also manifest Bronchioloalveolar carcinoma, for its part, is the most with hemorrhagic or nonhemorrhagic nodules. In the case common reason for the halo sign in immunocompetent of nonhemorrhagic nodules, the halo sign corresponds to patients14 (Figure 3). the presence of an inflammatory infiltrate, which normally The halo sign has also been associated with other affects the alveolar interstitium. histologic variants of primary lung tumors such as squamouscell carcinoma and mucinous cystadenocarcinoma.14,30 Pulmonary lymphomas can also manifest with areas of consolidation or as single or multiple pulmonary nodules Wegener granulomatosis is a form of granulomatous on CT scans.31 These nodules may be surrounded by a halo vasculitis that manifests with the classic triad of lung disease, in primary lymphomas (such as mucosa-associated sinusitis accompanied by fever, and necrotizing Figure 4. Pulmonary lymphoma in a 73-year-old patient who visited the emergency service with dyspnea. A: An axial scan of the lower pulmonary lobes
shows multiple pulmonary nodules with a halo sign and a tendency to coalesce in the posterior segments. There is also bilateral pleural effusion, somewhat
greater on the right side. The patient died 3 weeks after admission. Autopsy revealed lymphoma cells lysed by natural killer cells in several organs. B: Low-
magnification image of pulmonary nodule showing mainly peribronchovascular tumor cell infiltration and marked necrosis (hematoxylin-eosin, magnification

×4). C: A higher-magnification image of the periphery of the nodule shows the infiltration of tumor cells along the alveolar walls (arrows) (hematoxylin-
eosin, magnification
×10).
Arch Bronconeumol. 2008;44(7):386-92 Document downloaded from http://www.archbronconeumol.org, day 15/12/2014. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
PARRÓN M ET AL. THE HALO SIGN IN COMPUTED TOMOGRAPHY IMAGES: DIFFERENTIAL DIAGNOSIS AND CORRELATION WITH PATHOLOGY FINDINGS Figure 5. Wegener granulomatosis. A: Computed tomography scan showing 2 pulmonary nodules surrounded by a halo (arrows) and an area of consolidation
in the left lower lobe (asterisk), also with a halo sign. The patient, whose first symptom was hemoptysis, also had rapidly progressing glomerulonephritis.
B: Microscopic image showing inflammatory infiltration of the arterial wall with a multinucleated giant cell (arrow) and endothelial destruction (arrowheads)
(hematoxylin-eosin, magnification
×20).
glomerulonephritis, although the lung is the most commonly of a patient with pneumonitis due to subacute affected organ. The main histology findings are necrotizing hypersensitivity who developed bronchiolitis obliterans granulomas accompanied by a mixed-cell infiltrate of with organizing pneumonia, which manifested with nodular neutrophils, histiocytes, and eosinophils, and focal opacities corresponding to intraluminal polyps of necrotizing vasculitis of small and medium-sized vessels.
granulation tissue caused by the organizing pneumonia.38 Lung hemorrhage in this case is caused by necrotizing The halo was an indication of alveolar wall thickening vasculitis,35 and the CT halo sign corresponds to localized due to lymphocytic infiltration. bleeding around the central nodule2,3 (Figure 5).
Eosinophilic pneumonia can also manifest with Pulmonary endometriosis can also manifest as pulmonary nodules surrounded by ground-glass attenuation, hemorrhagic pulmonary nodules because even ectopic and in this case the halo is probably due to infiltration by endometrial tissue can bleed during menstruation.3 eosinophils and other inflammatory cells.3,14,39 Finally, there have been reports of lung transplant patients Nodules associated with pulmonary amyloidosis can presenting nodules surrounded by a CT halo following a also sometimes be surrounded by a halo, possibly reflecting transbronchial biopsy; the halo sign in these cases was the presence of nonspecific inflammatory cells, amyloid probably caused by bleeding due to biopsy injury.4 deposits on the peripheral alveolar walls, or both.
Moreover, the halo sign is a useful prognostic factor innodular pulmonary amyloidosis, as it is associated with faster disease progression and better response to Approximately 90% of patients with sarcoidosis develop lung disease. Histology findings typically include sarcoid Several lung disorders caused by amiodarone pulmonary granulomas, while CT findings include multiple small toxicity also manifest with nodules surrounded by a CT nodules (corresponding to sarcoid granulomas) with halo. Amiodarone can cause pneumonitis because its main predominant perivascular and subpleural distribution and metabolite, desethylamiodarone, interferes with lipid peribronchovascular interstitial and interlobular septal catabolism and induces generalized phospholipidosis, a thickening. Coalescing granulomas may also form irregular iatrogenic cause of endogenous lipoid pneumonia. The pseudonodules, an image referred to as the sarcoid galaxy halo seen on the CT scan may be due to the thickening of sign. There may also occasionally be areas of ground- the alveolar walls caused by a mixed inflammatory cell glass attenuation, sometimes surrounding the nodules.
infiltrate around a nodule of fibroblastic intraluminal Such areas are usually reversible and are believed to indicate polyps, which may mimic organizing pneumonia in sites other than the bronchioles.41 CT findings for organizing pneumonia include areas of consolidation or ground-glass attenuation, typically in subpleural or peribronchial areas, predominantly in thelower lobes. Some patients with organizing pneumonia A wide spectrum of diseases can manifest with a halo develop multiple nodules with an irregular margin and, on the CT chest scan. Although the halo sign is most often occasionally, a surrounding halo.13,37 There is also a report an indication of a hemorrhagic nodule, it may also Arch Bronconeumol. 2008;44(7):386-92 Document downloaded from http://www.archbronconeumol.org, day 15/12/2014. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.
PARRÓN M ET AL. THE HALO SIGN IN COMPUTED TOMOGRAPHY IMAGES: DIFFERENTIAL DIAGNOSIS AND CORRELATION WITH PATHOLOGY FINDINGS accompany other lesions such as inflammatory or tumor 16. Webb WR, Muller NL, Naidich DP, editors. High resolution CT of cell infiltrates. Consequently, while the halo sign is the lung. Philadelphia: Lippincott Williams & Wilkins; 2001. relatively nonspecific, it can be of great value for differential 17. Sbragia P, Falaschi F, Cambi L, Marinari A, Neri E, Fazzi P, et al.
The computerized tomography halo sign in a case of productive diagnosis. Such diagnosis, however, must be based on granulomatous pulmonary tuberculosis without intra and/or careful consideration of all the chest CT findings within extralesional hemorrhage. Radiol Med (Torino). 1996;92:649-50. the context of the patient's clinical state. Other CT findings, 18. Voloudaki AE, Kofteridis DP, Tritou IN, Gourtsoyiannis NC, Tselentis such as the number of nodules, the presence of diseased YJ, Gikas AI. Q fever pneumonia: CT findings. Radiology.
lymph nodes, or the discovery of pleural involvement can all help to narrow the diagnosis. The most likely diagnoses 19. Waldman AD, Day JH, Shaw P, Bryceson AD. Subacute pulmonary granulomatous schistosomiasis: high resolution CT appearances – that should be considered in immunosuppressed patients another cause of the halo sign. Br J Radiol. 2001;74:1052-5. are invasive pulmonary aspergillosis, viral pneumonia, 20. Nara M, Sasaki T, Shimura S, Yamamoto M, Oshiro T, Kaiwa Y, et Kaposi sarcoma, and lymphoma. In immunocompetent al. Diffuse alveolar hemorrhage caused by lung metastasis of ovarian patients, particular attention should be paid to viral angiosarcoma. Intern Med. 1996;35:653-6. infections and bronchioloalveolar carcinoma and other 21. Tomiyama N, Ikezoe J, Miyamoto M, Nakahara K. CT halo sign in metastasis of osteosarcoma. AJR Am J Roentgenol. 1994;162:468. 22. Pandit SA, Fiedler PN, Westcott JL. Primary angiosarcoma of the lung. Ann Diagn Pathol. 2005;9:302-4. 23. Gruden JF, Huang L, Webb WR, Gamsu G, Hopewell PC, Sides DM. AIDS-related Kaposi sarcoma of the lung: radiographic findingsand staging system with bronchoscopic correlation. Radiology.
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PARRÓN M ET AL. THE HALO SIGN IN COMPUTED TOMOGRAPHY IMAGES: DIFFERENTIAL DIAGNOSIS AND CORRELATION WITH PATHOLOGY FINDINGS 38. Herráez I, Gutiérrez M, Alonso N, Allende J. Hypersensitivity 40. Horger M, Lengerke C, Pfannenberg C, Wehrmann M, Einsele H, pneumonitis producing a BOOP-like reaction. HRCT/pathologic Knop S, et al. Significance of the "halo" sign for progression and correlation. J Thorac Imaging. 2002;17:81-3. regression of nodular pulmonary amyloidosis: radiographic- 39. Kang EY, Shim JJ, Kim JS, Kim KI. Pulmonary involvement pathological correlation. Eur Radiol. 2005;15:2037-40. ofidiopathic hypereosinophilic syndrome: CT findings in five patients.
41. Chouri N, Langin T, Lantuejoul S, Coulomb M, Branbilla C. Pulmonary J Comput Assist Tomogr. 1997;21:612-5. nodules with the CT halo sign. Respiration. 2002;69:103-6. Arch Bronconeumol. 2008;44(7):386-92

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