歐放精選(003):反暈徵的鑑別診斷要點

ECR 2017 / C-2304
Interpreting the reversed halo sign: differential characteristics and key clues.This poster is published under an open license. Please read the disclaimer for further details.Congress:ECR 2017Poster No.:C-2304Type:Educational ExhibitKeywords:Ischaemia / Infarction, Infection, Chronic obstructive airways disease, Diagnostic procedure, CT-High Resolution, CT, Thorax, Respiratory systemAuthors:B. Del Rio, M. D. Esteba-Bech-de-Careda, M. Ferrer, M. Torre, I. Romero Novo, J. L. Reyes Juarez; Terrassa/ESDOI:10.1594/ecr2017/C-2304DOI-Link:http://dx.doi.org/10.1594/ecr2017/C-2304Learning objectives

To learn to recognize the reversed halo sign and to know the spectrum of diseases in which it is seen.

 

To become familiar with the key findings that enable the differential diagnosis among conditions in which the reversed halo sign can occur.

Background

Voloudaki et al. initially described the presence of central annular ground-glass opacity surrounded by a peripheral rim of consolidation in a case report involving two COP cases. This finding was later called the 「reversed halo sign」 (RHS) when in 2003, Kim et al. concluded that it was disease specific from a series of confirmed cases of COP. However, by the time the RHS was included in the Fleischner Society Glossary of Terms in 2008, it had already been described in paracoccidioidomycosis, tuberculosis and certain vasculitides such as Wegener's disease, and from then on has been described in many other diseases.

 

Although not considered specific anymore, RHS recognition can be of great help to radiologists, because integrating morphological characteristics of the RHS, additional HRCT findings and patient clinical data can lead to a differential diagnosis that guides clinicians in their decision making.

 

 

In this paper, we describe the clinical and morphological data that could be useful for narrowing the differential diagnosis.

Findings and procedure details

Imaging findings

 

The reversed halo sign (RHS) is characterized by a focal rounded area of ground-glass opacity surrounded by a more or less complete ring of consolidation on high-resolution CT (HRCT). (1)

 

Fig. 1: Schematic representation of the reversed halo sign, with a central area of ground glass opacification surrounded by a rim of consolidation.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

Histopathologically, there are certain characteristics that are common in all cases. It is formed by an area of exclusively alveolar septal involvement in the ground-glass opacification (GGO) center of the node with entire-alveolus involvement in the peripheral consolidation ring. Although this involvement pattern remains constant, the anatomicopathological substrate of the RHS in each case depends on its cause.

 

Fig. 2: Schematic representation of the histopathology of the RHS, formed by an area of exclusively alveolar septal involvement in the ground-glass opacification (GGO) center of the node with entire-alveolus involvement in the peripheral consolidation ring.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

In some conditions, the RHS presents differential morphological characteristics, which, in combination with clinical data, may be key to diagnosis. Two differential morphological findings of RHS have been described: RHS with thickened rim and reticulation or 「bird nest sign」 in invasive fungal infections (IFI) and RHS with micronodules in active granulomatous diseases.

 

RHS with thickened rim and reticular GGO center

 

The reticular RHS is linked with invasive fungal disease and its differential findings are the reticular pattern in the  GGO center of the RHS and a peripheral condensation ring > 1cm thick. 

 

Fig. 3: A: 55-year-old man with leukemia after stem cell transplantation who presented with biopsy-proven pulmonary mucormycosis. CT image shows reversed halo sign in left upper lobe with thick peripheral rim of consolidation and subtle reticulation within central ground-glass component. Image courtesy of Dr. Edson Marchiori. Federal University of Rio de Janeiro, Rio de Janeiro, Brazil. B: RHS with thickened rim (>1cm) and reticular GGO center has been described in invasive fugal infection.
References: E. Marchiori et al. Can Morphologic Characteristics of the Reversed Halo Sign Narrow the Differential Diagnosis of Pulmonary Infections? AJR 2014; 203:557-558

 

In a comparative study of patients with IFI and patients with COP, Marchiori et al. describe central reticulation in 93% of patients with IFI and in no patients with COP. In addition, the maximum thickness of the condensation ring was 2.04±0.85 cm for IFIs while for the COP it was 0.5±0.22 cm. (2)

 

RHS with nodular rim and nodules in the GGO center

 

RHS with micronodules is related to active granulomatous diseases, mainly tuberculosis, but also to other granulomatous diseases, such as paracoccidioidomycosis or cryptococcosis and non-infectious granulomatous diseases such as sarcoidosis. (3) Differential characteristics in this case include the finding of a nodular peripheral ring and micronodules within the GGO center of the RHS.

 

Fig. 4: A: 59-year-old woman with pulmonary tuberculosis. High-resolution CT image of lower right pulmonary region shows bilateral random nodules and reversed halo sign on lower lobe. Note that halo walls are nodular and the GGO center has micronodules. Image courtesy of Dr. Edson Marchiori. Federal University of Rio de Janeiro, Rio de Janeiro, Brazil. B: RHS with nodular rim and micronodules in the GGO center related to active granulomatous diseases.
References: E. Marchiori et al. Can Morphologic Characteristics of the Reversed Halo Sign Narrow the Differential Diagnosis of Pulmonary Infections? AJR 2014; 203:557-558

 

In another comparative study, in this case involving patients with tuberculosis and COP, Marchiori et al. found nodular borders in all tuberculosis patients and central micronodules in 83%, while these findings were not apparent in any of the COP patients. (4)

 

However, in the majority of cases, the RHS lacks specific findings. It is essential to identify the key data from the patient’s clinical situation so that an approximate diagnosis can be made. We describe various clinical situations that can guide the radiologist after the finding the RHS.

 

The Clinical Data: Key Clues

 

Fig. 5: Mind map for the differential diagnosis of the reversed halo sign
References: Consorci Sanitari Terrassa - Terrassa/ES

 

 

Clinical signs and symptoms of pulmonary infection

 

The RHS is presented in a broad spectrum of infectious pulmonary diseases, therefore the patient’s clinical data is helpful to lead the differential diagnosis.

 

Severe immunosuppression and neutropenia: Invasive Fungal Pneumonia

 

In severely immunosuppressed and neutropenic patients (5), patients with hematological malignancies, patients in aggressive chemotherapy cycles or in the course of a bone marrow transplant, opportunistic fungal diseases have to be included in the differential diagnosis.

In these patients, the RHS is an early sign that translates an area of pulmonary infarction with greater peripheral hemorrhagic component, which can later cavitate. Histologically, in the central area of the RHS, there are multiple arterioles and venules occluded by hyphae, while the peripheral ring is formed of inflammatory fibrinous exudates and pulmonary hemorrhage.

The most frequent IFP is angioinvasive aspergillosis (AIA), however, in the presence of RHS, pulmonary mucormycosis (PM) should be considered the most probable diagnosis. PM is another opportunistic fungus that in 19% of cases presents RHS, compared with <1% of cases of AIA. (6)  Other data that may help us with the diagnosis of PM are the presence of sinusopathy, multiple (>10) pulmonary nodules, and pleural effusion, (as well as a lack of response to voriconazole). (7)

 

Recently traveled to endemic mycoses areas: Paracoccidioidomycosis, cryptococcosis and histoplasmosis.

 

The RHS has been described in up to 10% of patients with Paracoccidioidomycosis (PCM). PCM is in the most frequent endemic mycosis in Latin America; the most seriously affected areas are the subtropical, rural areas of Brazil, where it can affect 10% of the population. Histologically, the RHS in these patients corresponds to a central area of inflammatory infiltrate in the alveolar wall, with preservation of the alveolar spaces, while an area of dense intra-alveolar inflammatory infiltrate forms the peripheral consolidation. (8)

 

The RHS has also been described in other endemic mycoses, such as cryptococcosis or histoplasmosis, which are related to contact with bird and bat droppings.

 

Tuberculosis risk factors: Tuberculosis

 

In patients from areas with high rates of  tuberculosis (TB), who live in an institution or in overcrowded conditions, who have been in contact with infectious TB patients or who are malnourished, TB should always be included in the differential diagnosis.

The RHS has also been described in post-primary TB. In these cases of RHS, the peripheral ring is composed of multiple nodules and in the center, micronodules are present in ground-glass density. Other findings associated with TB are: tree-in-bud centrilobular nodules, bronchial wall thickening, consolidation, cavitated lesions and lymphadenopathy.  (9)

 

AIDS: Pneumocystis Jiroveci Pneumonia

 

Pneumocystis Jiroveci Pneumonia (PJP) is the most common opportunistic infection in in patients with acquired immunodeficiency syndrome (AIDS). Although the RHS is rare in these patients, PJP should be considered in the differential diagnosis. (7) (10)

 

Recent bacterial pneumonia

 

The RHS has been described in the late-resolution phase of bacterial, pneumococcal, psittacosis or legionella pneumonias. However, it is not clear whether this corresponds to a specific bacterial disease or if it is part of a secondary organizing pneumonia, triggered by the inflammatory damage caused by the infection. (11)

 

Fig. 6: 50 year-old male with secondary organising pneumonia in the recovery fase of a mycoplasma pneumonia. HRCT shows multiple patchy areas of consolidation of subpleural and peribroncovascular distribution, and multiple images of reversed halo sign.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

 

Known primary neoplasm

 

Recent radiofrequency ablation of lung nodules:  Changes after radiofrequency ablation

 

Fig. 7: A: CT image obtained during the radiofrequency ablation (RFA) session shows the RF needle in the treatment place. B: CT inmediately after RFA demonstrates a ground-glass halo surrounding the lesion, consistent with postreatment changes, and a small pneumothorax. The linear RFA tract is identified. C: CT image obtained 6 weeks after RFA shows a peripheral consolidation with central ground-glass opacity, consistent with the reversed halo sign. Moderate pleural thickening and an small cavitated lesion in the center of the RHS is visible. D: Coronal CT image of the same lesion. Images courtesy of Dr. Xavier Gallardo from UDIAT-CD, Hospital Universitari Parc Tauli (Sabadell, Barcelona).
References: UDIAT-CD. Hospital Universitari Parc Tauli (Sabadell, Spain)

 

The RHS has been described as an early secondary finding (in the first 1-3 months) of radiofrequency ablation of pulmonary nodules. According to Mango et al., the central GGO area would correspond to an area of coagulative necrosis of the nodule and surrounding healthy tissue, whereas peripheral consolidation would correspond to fibrotic tissue with inflammatory cells. Other findings related to radiofrequency ablation would be the appearance of a GGO area in the surrounding healthy parenchyma, cavitation of the treated area and pleural thickening at the puncture site. (12).

 

Recent radiotherapy on pulmonary parenchyma:  Radiation-induced lung disease

 

The RHS has been described in the acute phase of radiation-induced lung disease (RILD), in the first 4-12 weeks after completing treatment. When it appears at the location of the treated nodule, it is considered linked to the tumor necrosis, whereas when it appears inside the radiation area but in healthy pulmonary parenchyma, it is related to inflammation or necrosis, which is secondary to radiation damage, or to outbreaks of organizing pneumonia triggered by pulmonary insult. Other early RILD findings are: GGO areas and consolidation in treated areas. (7)

 

On-going or recent chemotherapy: Drug toxicity.

 

Fig. 8: Pneumonitis in a 62-year-old male with lung adenocarcinoma in treatment with Nivolumab. CT images demonstrate areas of GGO with peripheral consolidation consistent with RHS in the peribronchovascular region of left upper lobe, left lower lobe and small foci at right lower lobe.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

In patients with neoplastic disease who have started chemotherapy, the finding of multiple RHS lesions may correspond to NSIP or organizing pneumonia secondary to drug toxicity. (7) We present the finding of RHS  in a patient with lung neoplasm treated with immunomodulators and without previous lung lesions. The RHS lesions remitted rapidly after treatment cessation and the administration of corticosteroid therapy. Fig. 9

 

Fig. 10: Pneumonitis in a 67 years-old female with breast cancer and a left lung mass treated wih Eribulin. CT scan shows bilateral patchy areas of GGO with a peripheric rim of consolidation, consistent with RHS.
References: Consorci Sanitari Terrassa - Terrassa/ES

Progression of the neoplastic disease: Metastasis

 

The appearance of new RHS lesions in a patient with a known tumor, not meeting any of the above criteria, should lead to a suspicion of lung metastatic progression. (7).  Although the RHS is a rare presentation form for lung metastases, it can translate a lepidic growth of tumor cells in the alveolar walls or an area of parenchymal infarction as a result of tumor emboli. (13)

 

Patient with vascular or thromboembolic disease

 

Pulmonary embolism: Pulmonary infarction

 

The RHS in patients with signs of pulmonary embolism (PE), particularly if both occur in the same lung segment, may translate an area of pulmonary infarction. Fig. 11  These lesions usually have a pleural base with an ellipsoid or pyramidal shape and appear in cases of subtotal PE, segmental and subsegmental branches, rather than massive or lobar PEs. Histopathologically, the RHS in pulmonary infarction translates an area of parenchymal hemorrhage with a viable central area of pulmonary parenchyma. Areas of pulmonary infarction heal by centripetal organization, so the lesions will decrease in size until they form linear scars. (14) (15)

 

Fig. 11: Acute pulmonary embolism with pulmonary infarction in a 47 year-old male. A: CT image (mediastinal window settings) shows a clot in the right middle and inferior and left inferior lobar arteries. B: CT image shows the reversed halo sign in the lateral segment of the right middle lobe and a small area of parenchymal consolidation in the superior segment of right lower lobe due to pulmonary infarction.
References: Consorci Sanitari Terrassa - Terrassa/ES

Fig. 12: Acute pulmonary embolism with pulmonary infarction in a 55 year-old female. A: CT image shows the reversed halo sign in the lateral segment of left upper lobe and lingula. B: CT image (mediastinal window settings) shows clots in the lingular and basal segmental arteries. C,D: Coronal and axial CT images showing triangular opacity of ground-glass density and peripheral consolidation in the basal segments of the left lower lobe.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

Vasculitis: Wegener's

 

The RHS has been described in patients with Wegener's granulomatosis. Wegener's granulomatosis is a necrotizing vasculitis, affecting small vessels. In these patients, the HRS can be seen during the intermediate stages of the affectation and in many cases, it evolves to cavitation. (16) In these cases, the RHS would probably translate an area of organizational reaction around an area of focal pulmonary hemorrhage. (17)

 

Asymptomatic patient or with subacute clinical symptoms

 

Adenocarcinoma with lepidic pattern

 

Pulmonary adenocarcinoma presents in numerous ways, as a single node or as multiple nodules, solid, subsolid or in GGO. The RHS is an uncommon presentation of lung adenocarcinoma where the GGO area is associated with a lepidic growth pattern in either an in situ adenocarcinoma or an invasive lepidic adenocarcinoma. (7) (18)

 

Lymphomatoid granulomatosis

 

Lymphomatoid granulomatosis (LG) is a rare extranodal lymphoproliferative disorder associated with Epstein-Barr virus (EBV), which mainly affects the lungs, but can also affect the kidney, liver, brain or skin. Histopathologically, EBV-positive atypical B-cell infiltrates are observed with an exaggerated proliferation of T cells in arterioles and medium-sized venules. (19) In this case, the RHS corresponds to areas of aerated parenchyma with a peripheral ring of lymphomathoid vascular invasion. (20) The main findings in LG are multiple peribronchovascular and septal infiltrative nodules that correspond to angiocentric granulomatous inflammation that may disappear, migrate or even evolve to areas of pulmonary infarction. (21)

 

Sarcoidosis

 

RHS has been described as an atypical sign in sarcoidosis. Sarcoidosis is a granulomatous disease of unknown etiology, with thoracic involvement in 90% of cases.  Its most frequent findings are bilateral hilar and right paratracheal nodal enlargement, which might associate with pulmonary involvement. Common parenchymal features are multiple perilymphatic nodules that predominate in the upper lobes with a subpleural or peripheral disposition and in fissures.

In their presentation of a case of sarcoidosis with RHS, Kumazoe et al. describe small nodules in both the GGO area and the peripheral consolidation ring. The histopathological correlation showed non-caseating granulomas, with no signs of parenchymal organization. (22) However, in another case of RHS in sarcoidosis presented by Fuji et al., the histopathological analysis demonstrated organizing pneumonia, secondary to sarcoidosis.  (7)

 

Cryptogenic Organising Pneumonia (COP)

 

Fig. 13: 19 year-old male with fever, cough, disnea and constitutional syndrome that after excluding other diseases was diagnosed with cryptogenetic organizing pneumonia. The CT scan shows multiple consolidative opacities with the reversed halo sign in a peribronchovascular distribution. The patient was treated with steroids with resolution of the lesions.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

The RHS was initially described in (COP), an idiopathic form of organising pneumonia, which remains a diagnosis of exclusion. COP remains the most common condition described in immunocompetent patients with RHS. Histopathologically, the GGO central area corresponds to an area of the alveolar wall inflammation with cellular debris, whereas, the peripheral consolidation ring responds to organising pneumonia within the alveoli. The most frequent findings in HRCT in COP are patchy areas of GGO, subpleural and peribroncovascular consolidations and nodules or masses with air bronchogram. (23) This features can also be found in secondary organising pneumonia.

 

Fig. 14: 66-year-old male with secondary organizing pneumonia three months after dropping Nivolumab treatment. High-resolution CT scan shows patchy pseudonodular areas of GGO with an outer rim of consolidation (reversed halo sign) predominating in the upper lobes and upper segments of lower lobes.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

Lipoid Pneumonia

 

The RHS has been described by Kanaji et al. in a case of exogenous lipoid pneumonia after inhaling spray paint. However, given the time elapsed since the diagnosis of pneumonia and the occurrence of the RHS on the HRCT (5 months), it cannot be ruled out that the RHS corresponded to organising pneumonia secondary to inflammation caused by lipoid pneumonia. (24)

 

Non-Specific Interstitial Pneumonia

 

NSIP is a chronic interstitial lung disease that may be related to collagen alterations, drug toxicity, hypersensitivity pneumonitis or may be idiopathic. In NSIP, the RHS is an uncommon sign that translates a state of inflammation with infiltration of the alveolar septa and preservation of the pulmonary architecture. (25)  The most common manifestation of NSIP is GGO that tend to predominate in the middle and lower lung. Other parenchymal features are irregular linear or reticular densities, areas of consolidation and traction bronchiectasies.

 

Chronic Eosinophilic Pneumonia (CEP)

 

Fig. 15: 50 year-old female with biopsy proven chronic eosinophilic pneumonia. Clinical history of cough, dispnea and rhinitis. HRCT shows areas of GGO predominating in the upper lobes and multiple difuse RHS images with peripheral distribution. The patient was treated with steroids with resolution of the lesions.
References: Consorci Sanitari Terrassa - Terrassa/ES

 

The RHS has been described in Chronic Eosinophilic Pneumonia, a chronic disease characterized by an eosinophilic infiltration of the pulmonary parenchyma.  In this case, the mechanism is considered likely to be similar to that of NSIP. Other CEP findings include peripheral parenchymal condensations, in the photographic negative of acute pulmonary edema. (26)

Conclusion

The RHS is easy to recognize and it can be found in a wide range of pathologies

In some cases, the RHS shows morphological characteristics that increase its specificity. When the RHS presents a reticular GGO center with a thickened peripheral rim (> 1cm), it is related to invasive fungal disease. When the RHS presents nodules in the ring or its interior, it is associated to active granulomatous diseases.

 

However in the majority of cases the RHS is a non-specific finding and clinical data and the patients's history should be considered in order to narrow the differential diagnosis.

Personal information

Belén del Río. Consorci Sanitari de Terrassa (Terrassa, Barcelona)

E-mail: [e-mail]

References

1. D. M. Hansell et al. Fleischner Society: Glossary of Terms for Thoracic Imaging. Radiology 2008; 245:697-722

 

2. E. Marchiori et al. Reversed Halo Sign in Invasive Fungal Infections Criteria for Differentiation From Organizing Pneumonia. AJR 2011; 197:1324–1327

 

3. E. Marchiori et al. Reversed Halo Sign High-Resolution CT Scan Findings in 79 Patients. CHEST 2012; 5: 1260-1266.

 

4. E. Marchiori et al. Reversed halo sign in active pulmonary tuberculosis: criteria for differentiation from cryptogenic organizing pneumonia. AJR 2011; 197: 1324-1327.

 

5. E. Marchiori et al. The Reversed Halo Sign on High-Resolution CT in Infectious and Noninfectious Diseases. AJR 2011; 197: 69–75.

 

6. S. P. Georgiadou et al. The Diagnostic Value of Halo and Reversed Halo Signs for Invasive Mold Infections in Compromised Hosts. Clinical Infectious Diseases 2011; 52: 1144–1155.

 

7. M. C. B. Godoy et al. The reversed halo sign: update and differential diagnosis. The British Journal of Radiology 2012; 85; 1226–1235.

 

8. E.L. Gasparetto et al. Reversed Halo Sign in Pulmonary Paracoccidioidomycosis. AJR 2005; 184: 1932–1934.

 

9. E. Marchiori et al. Pulmonary tuberculosis associated with the reversed halo sign on high-resolution CT. The British Journal of Radiology 2010; 89: 58-60.

 

10. H. Otera et al. Reversed halo sign in pneumocystis pneumonia: a case report. BMC Medical Imaging 2010; 26.

 

11. V. Tzilas et al. The 「reversed halo」 sign in pneumonococcal pneumonia: a review with a case report. European Review for Medical and Pharmacological Sciences 2010; 14: 481-486.

 

12. V. L. Mango et al. Reversed Halo Sign After Radiofrequency Ablation of a Lung Nodule. Journal of Thoracic Imaging 2011; 26: 150-152.

 

13. J. B. Seo et al. Atypical Pulmonary Metastases: Spectrum of Radiologic Findings. Radiographics 2001; 21: 403–417.

 

14. J. Casullo et al. Reversed halo sign in acute pulmonary embolism and infarction. Acta Radiológica 2013; 54: 505-510.

 

15. J. Balakrishnan et al. Pulmonary Infarction: CT Appearance with Pathologic Correlation. Journal of Computer Assisted Tomography 1989; 13: 941–945.

 

16. R. Agarwal etbal. Another cause of reverse halo sign: Wegener’s granulomatosis. The British Journal of Radiology 2007; 80: 849-850.

 

17. L. Ananthakrishnan et al. Wegener’s Granulomatosis in the Chest: High-Resolution CT Findings. AJR 2009; 192: 676-682.

 

18. MC. Godoy et al. Subsolid pulmonary nodules and the spectrum of peripheral adenocarcinomas of the lung: recommended interim guidelines for assessment and management. Radiology 2009; 253: 606–622.

 

19. JS. Lee et al. Lymphomatoid Granlomatosis: radiologic features and pathologic correlations. AJR 2000; 175: 1335-1339.

 

20. RE. Benamore et al. Reversed halo sign in lymphomatoid granulomatosis. The British Journal of Radiology 2007; 80:162-166.

 

21. VN. Maturu et al. Reversed Halo Sign: A Systematic Review. Respiratory Care 2014; 9:1-10

 

22. H. Kumazoe et al. 『『Reversed halo sign』』 of high-resolution computed tomography in pulmonary sarcoidosis. J Thorac Imaging 2009; 24: 66-68.

 

23. SJ. Kim et al. Reversed Halo Sign on High-Resolution CT of Cryptogenic Organizing Pneumonia: Diagnostic Implications. AJR 2003; 180:1251-1254.

 

24. N. Kanajia et al. Lipoid pneumonia showing multiple pulmonary nodules and reversed halo sign. Respiratory Medicine Extra 2007; 3: 98-101.

 

25. SH. Hong et al. Reversed halo sign on thin-section CT in a patient with non-specific interstitial pneumonia.The British Journal of Radiology 2011; 84: 103-105.

 

26. M. Gholamnejad et al. Unusual Presentation of Chronic Eosinophilic Pneumonia with 「Reversed Halo Sign」: A Case Report. Iran J Radiol 2014; 11:7891

歐放精選（002）：前列腺及前列腺周圍囊腫：具有挑戰性的診斷

歐放精選（001）：彌散受限的顱內非血管性病變

ECR2010：慢性肺實變的影像學表現及鑑別診斷

ECR2017 : Dilated Pancreatic Duct

ECR2011：時間分辨MRDSA平掃直接顯示硬腦膜動靜脈瘻

FROM：http://dx.doi.org/10.1594/ecr2017/C-2304

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