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Ground glass opacity on CT scanning of the chest: What does it mean?

Jannette Collins, MD and Eric J. Stern, MD

G

round glass opacity (GGO) is described as a “hazy increased attenuation of lung, with preservation of bronchial and vascular margins; it is caused by partial filling of air spaces, interstitial thickening, partial collapse of alveoli, normal expiration, or increased capillary blood volume.”1 GGO is a nonspecific finding, and the differential diagnosis of the many causes of GGO can be lengthy. An “ABCs” approach and a “pattern” approach to the interpretation of GGO on HRCT scanning of the lungs have previously been described.2,3 This paper provides an abbreviated review of the physiologic correlates of the HRCT scan findings of GGO, focusing on infiltrative processes and their different GGO patterns of presentation. GGO can be patchy, resulting in a mosaic pattern of lung attenuation. Such a pattern can be seen in infiltrative lung disease, airway abnormalities (e.g., asthma, bronchiolitis obliterans), and chronic pulmonary vascular disease (e.g., chronic thromboembolic disease).4 The distinction between these three entities can be made by observing the size of the pulmonary vessels in the area of increased lung attenuation (increased in both airway disease and vascular disease, but not in infiltrative disease), and by examining air trapping on expiratory scans (indicating airway disease) (figure 1).
Dr. Collins is in the Department of Radiology at the University of Wisconsin Hospital and Clinics, in Madison, WI. Dr. Stern is in the Department of Radiology at Harborview Medical Center, University of Washington in Seattle, WA.

Pitfalls in the interpretation of GGO on CT scanning
As recognition of GGO is based on a subjective assessment of lung attenuation, it is important to understand the parameters that can interfere with lung density and make attenuation measurements unreliable.5,6 Window widths and levels that are too narrow can erroneously create the appearance of GGO by artificially “blooming” small structures. In evaluating for GGO, collimation ideally should be 1.0 to 1.5 mm. True GGO can not always be visualized with a thicker collimation because of volume averaging, and a thicker collimation sometimes results in a pseudo-GGO pattern. GGO is therefore best imaged with high-resolution CT (HRCT). Lung attenuation normally increases homogeneously with expiration. This increased attenuation can obscure underlying pathologic GGO. Furthermore, if the expiratory nature of the

examination is not recognized, an erroneous interpretation of pathologic GGO can be made. Cardiac and respiratory motion also can create pseudo-GGO, which can be distinguished from pathologic GGO by recognizing the blurring and double images of vessels and fissures. GGO in the gravity dependent portions of the lungs is often seen as a result of microatelectasis, which can be differentiated from pathologic GGO by re-scanning the area of question with the patient in the prone position.

Infiltrative processes resulting in GGO
Many patterns of distribution of ground glass opacity can be seen on HRCT of the lungs. It is important to emphasize that most such disease processes can and do result in more than one pattern, often simultaneously; the patterns change depending upon the acuity or chronicity of the disease

A

B

FIGURE 1. Asthma. Image shows a 20-year-old woman with wheezing and shortness of breath responsive to bronchodilator treatment. (A) Inspiratory HRCT (1.0 mm collimation) was normal. (B) Expiratory HRCT (1.0 mm collimation) shows a mosaic pattern of lung attenuation. The areas of increased attenuation represent normal lung during expiration, while the adjacent abnormal lucent areas of lung represent air trapping. This pattern of air trapping on expiratory scanning, without associated abnormalities, is seen most often with obliterative bronchiolitis and asthma (small airways diseases), and should be differentiated from infiltrative processes where areas of GGO are seen on the inspiratory images and mosaic attenuation is not accentuated on expiratory imaging.

APPLIED RADIOLOGY, December 1998

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CT scan findings of ARDS include bilateral and gravitydependent lung opacities. FIGURE 5. contusion. of which there are many. December 1998 . Helical CT scan (10 mm collimation) shows diffuse bilateral GGO. primarily to inhaled organic antigens. ings in patients with hydrostatic pulmonary edema include areas of GGO. The main differential diagnosis in this group of patients is cytomegalovirus pneumonia. correlating with the clinical diagnosis of acute farmer’s lung. interlobular septal thickening. HRCT (1. HRCT is reported to be 65% sensitive and 85% specific in making the diagnosis of acute rejection in the lung transplant population. We have categorized the etiologies of GGO according to the most commonly seen patterns of distribution: Diffuse pattern of GGO—Disease processes commonly resulting in a diffuse pattern of GGO on CT scanning are listed in table 1. commonly accompanied by GGO and interlobular septal thickening. infection. which is patchy and localized in mild rejection and widespread in severe rejection (figure 2). subacute. These leaks lead to extravasation of protein-rich fluid into the interstitial and alveolar spaces of the lung. The patient went on to develop severe ARDS with complications of barotrauma. increased capillary permeability.11 The distribution of GGO can be diffuse. The clinical presentation may be acute.0 mm collimation) shows diffuse bilateral GGO. A 45-year-old man presents with increasing shortness of breath 2 months after bone marrow transplantation. and rejection can be difficult both clinically and radiographically. differentiating between reperfusion edema. In the acute and subacute phases. CT shows 1. small nodules (55%).Causes of a diffuse pattern of GGO on CT scanning • Acute rejection of lung transplantation • Adult respiratory distress syndrome • Edema • Extrinsic allergic alveolitis • Hemorrhage • Infectious pneumonia Table 1 FIGURE 2. In the subacute phase. HRCT (1. Among the common causes of ARDS are aspiration. peribronchovascular interstitial thickening.12 In the acute phase. also called hypersensitivity pneumonitis. Acute rejection is common after lung transplantation. increased vascular caliber. and air trapping.10 Extrinsic allergic alveolitis. or chronic. requiring intubation and mechanical ventilation after receiving chemotherapy for lymphoma.11 GGO correlates histologically with mononuclear cell infiltration of the alveolar walls.. or centrilobular (figure 4) in this condition. correlating with a pathologic diagnosis of severe acute rejection. and transbronchial lung biopsy and bronchoalveolar lavage showed no evidence of infection. a reticular pattern (36%). viral. mycobacterial. Early adult respiratory distress syndrome (ARDS). A 38-year-old man presents with increasing shortness of breath 3 weeks after bilateral lung transplantation. CMV is the most common viral pathogen to cause substantial mor- 18 APPLIED RADIOLOGY. depending on the underlying cause. A 12-year-old boy with acute shortness of breath and hypoxemia. A diffuse pattern of GGO in the absence of associated CT scan findings is a characteristic presentation for cytomegalovirus pneumonia (CMV) and Pneumocystis carinii pneumonia (PCP). fungal. However. FIGURE 4. which can have an identical radiographic appearance. Acute rejection of lung transplantation.5 HRCT scan find- FiGURE 3. Adult respiratory distress syndrome (ARDS) is a form of nonhydrostatic pulmonary edema. and thickening of fissures. patchy. Diffuse alveolar hemorrhage.0 mm collimation) shows diffuse bilateral GGO. bacterial. which persists on follow-up CT in 50% of patients (figure 3).9 Both cardiogenic and non-cardiogenic edema occurs when the capacity of the lung lymphatics to drain capillary transudate is exceeded. and sepsis. all patients demonstrate GGO on CT. CT scans show consolidation or GGO (figure 5).g. Pulmonary artery wedge pressure was normal.13 Infectious pneumonia of any cause (e. or focal. HRCT (1. Extrinsic allergic alveolitis. smoke inhalation. process. Etiologies include venous and lymphatic obstruction. HRCT scan findings will vary with the stage of disease.0 mm collimation) shows diffuse bilateral GGO. pleural effusion.8 Early in the course of ARDS. and parasitic) can cause GGO to appear on HRCT scans. and hypoproteinemia.to 3-mm nodules that are distributed in a uniform fashion. patchy. is a complex immunologic reaction by the lung.7 The only significant HRCT finding in acute rejection (seen in 65% of these patients) is GGO. Imaging of a 50-year-old farmer with an acute onset of increasing shortness of breath. characterized by leaky capillary membranes. Pulmonary hemorrhage can be diffuse. findings include GGO (in 82%).

also may result in a focal pattern of GGO. Focal GGO patterns—There is overlap between causes of diffuse. trauma. Pneumocystis carinii pneumonia in a 39-year-old man with AIDS. Image is of a 49-year-old man with acute myelogenous leukemia and fever.14 and is a relatively common complication in organ transplant recipients.16 Patchy GGO patterns—Many of the causes of a patchy distribution of GGO on HRCT scanning. or pulmonary infarction. but not pathognomonic. bronchial wall thickening or bronchiectasis.23 The GGO represents a Causes of a focal pattern of GGO on CT scanning • Bronchiolitis obliterans organizing pneumonia (BOOP) • Bronchoalveolar lavage • Bronchioloalveolar cell carcinoma • Hemorrhage • Pulmonary infection Table 3 APPLIED RADIOLOGY. plasm.Causes of a patchy pattern of GGO on CT scanning • Acute rejection of lung transplantation • Adult respiratory distress syndrome • Bronchiolitis obliterans organizing pneumonia (BOOP) • Bronchioloalveolar cell carcinoma • Extrinsic allergic alveolitis • Hemorrhage • Infectious pneumonia • Pulmonary alveolar proteinosis Table 2 bidity and mortality in patients with AIDS.21 Other processes that can show a crazy paving pattern at HRCT scanning include ARDS. especially if the GGO is observed in the right middle lobe or lingula. When pulmonary hemorrhage is due to focal neo- FIGURE 6. creating the “halo sign”. Small bilateral pleural effusions are present. GGO. and focal distributions of GGO (table 3) with chest CT scanning. dense consolidation. Spain.15 In organ transplant recipients with CMV pneumonia. lipoid pneumonia.0 mm collimation) shows bilateral patchy areas of GGO with a background of intralobular and interlobular septal thickening. The surrounding GGO. Lipoid pneumonia. The technique involves injection of normal saline through a bronchoscope that is generally wedged into the lingular or middle lobe bronchus. areas of septal thickening (straight arrows).” and is characteristic. In patients with AIDS and CMV pneumonia. with an overlying branching pattern of white linear structures forming geometric shapes and outlining polygonal. a focal pattern of opacity results. Bronchoalveolar lavage is a procedure used to diagnose pulmonary diseases and to identify predictors of prognosis. Most. Image is of a 46-year-old man with a 6-month history of mild dyspnea and chronic rhinitis. Helical CT scan (10 mm collimation) shows diffuse bilateral GGO. represents hemorrhage and is highly specific for early invasive aspergillosis in leukemic patients. and square forms. and ill-defined small nodular opacities (curved arrows). may also result in a diffuse pattern of GGO. Table 4 lists the processes known to produce the halo sign. producing the “crazy paving” pattern first described with alveolar proteinosis.5 mm collimation) shows patchy bilateral areas of GGO and a small cystic lesion in the left upper lobe (arrows).22 The residual fluid demonstrates a segmental or lobar distribution of GGO on CT scanning. Invasive aspergillosis. triangular.) FIGURE 7. consolidation.19. Imaging of a 42-year-old man with acute respiratory symptoms 3 months after bone marrow transplantation. consolidation. It was first reported as a sign of early invasive pulmonary aspergillosis in patients with leukemia. HRCT (1. such as lobar pneumonia. FIGURE 8. The presence of an isolated ground glass infiltrate without additional findings in patients with AIDS is highly suggestive of PCP(figure 7). Cytomegalovirus pneumonia. treated with oily nose drops. (Figure courtesy of Tomas Franquet.0 mm collimation) shows a triangular area of consolidation abutting the peripheral right lung and involving both the right middle and lower lobes. HRCT (1. Pulmonary alveolar proteinosis is a disease of the lung that results in filling in of the alveoli by a periodic acidSchiff-positive proteinaceous material that is rich in lipid. but not all of the fluid is aspirated back into the scope and examined for inflammatory and immune mediator cells and specific proteins.18 HRCT scanning of this disorder shows GGO. Barcelona.5 The “halo” pattern of GGO—A “halo” of GGO occasionally can be seen around a nodule or focal area of lung FIGURE 9. patchy. and irregular lines (figure 6).17. MD. Helical CT scan (7. Certain infections. CT scanning will show GGO. listed in table 2. of the diagnosis of alveolar proteinosis (figure 8). This distribution and shape is characteristic of hemorrhagic infarction caused by the angioinvasive fungal agent aspergillosis. and PCP. December 1998 19 .20 This pattern is often referred to as “crazy paving. CT scanning shows small nodules. which should suggest the possibility of recent bronchoalveolar lavage. and interstitial reticulation without air-space disease (although GGO may occur in isolation).

These pseudo nodules have been described in Causes of a “halo” pattern of GGO on CT scanning • Invasive pulmonary aspergillosis • Neoplasm. Helical CT scan (10 mm collimation) shows bilateral areas of GGO and consolidation in a typical peripheral non-segmental distribution. CT scanning shows nodular areas of GGO and consolidation. There are both posterior and anterior rib fractures adjacent to the sites of contusion. GGO is seen on CT scanning in 63 to 100% of these patients. rheumatoid arthritis. polymyositis/dermatomyositis. December 1998 .25 but they may be seen in any patient after lung biopsy.24 In most patients.27-29 Collagen vascular diseases are multisystem disorders characterized by vascular changes. A peripheral pattern of GGO— Processes that are known to result in a peripheral lung distribution of GGO with HRCT scanning are listed in table 5. results in a similar distribution of GGO on CT scanning but typically with more areas of honeycombing and traction bronchiectasis (figure 13).31 Pulmonary contusion results from trauma to the chest wall and lung. Desquamative interstitial pneumonitis. consolidation. HRCT (1. peripheral ring of hemorrhage or hemorrhagic infarction surrounding target lesions of pulmonary aspergillosis (figure 9). systemic lupus erythematosus.35.36 Pulmonary eosinophilia occurs with a variety of conditions or diseases. the cause is a compression injury with significant kinetic energy absorption adjacent to the site of chest wall injury. bilateral.37 Acute idiopathic eosinophilic pneumonia is characterized by diffuse GGO and micronodules on chest radiographs and CT scans. The HRCT scan findings consist of GGO with a lower lung zone (73%) and a peripheral (59%) predominant distribution (figure 12). or both. Specific diseases include progressive systemic sclerosis (scleroderma).30 and is a sign of active inflammation in the absence of significant honeycombing. Usual interstitial pneumonitis. and organizing pneumonia extending into the surrounding alveoli. nodules. Chronic idiopathic eosinophilic pneumonia is characterized by multiple dense areas of opacity on chest radiographs and CT scans. Several infectious and noninfectious causes of the CT halo sign have since been reported.38 20 APPLIED RADIOLOGY. HRCT (1. or areas of consolidation with a predominantly peripheral (50% of patients). In one study of patients with chronic eosinophilic pneumonia. Another cause of focal GGO. especially when combined with other clinical data and associated CT scan findings. often in a bronchovascular distribution. or idiopathic pulmonary fibrosis. and Sjogren’s syndrome. Image is of a 50-year-old man with increasing shortness of breath after bilateral lung transplantation. fibrosis.26 CT scans show patchy GGO (in 8 to 75% of patients). hemorrhagic • Post-biopsy pseudo nodule Table 4 patients who have undergone lung transplantation and transbronchial lung biopsy. or a nodule with a surrounding halo of GGO. Pulmonary toxicity has been associated with numerous drugs and a variety of radiographic and CT patterns. Image is of a 77-year-old man with a 3-month history of increasing shortness of breath. or can be idiopathic. Generally. often with a peripheral distribution. the most common HRCT finding was GGO.5 mm collimation) shows bilateral areas of GGO and consolidation in a peripheral distribution without evidence of honeycombing or traction bronchiectasis. is the post-biopsy pseudo nodule. and inflammation of connective tissue. or other signs of lung fibrosis. nonanatomic distribution (figure 11). usually with a peripheral. FIGURE 12. hemorrhagic nodules can be distinguished from nonhemorrhagic nodules by the presence of a halo of GGO. with bleeding into the air spaces and lung interstitium. Image is of a 22year-old man involved in a motor vehicle accident. and nonsegmental distribution (figure 10). Contusions. FIGURE 11.32.Causes of a peripheral pattern of GGO on CT scanning • Bronchiolitis obliterans organizing pneumonia (BOOP) • Collagen vascular disease • Contusion • Desquamative interstitial pneumonitis • Drug toxicity • Eosinophilic pneumonia • Fibrosis • Sarcoidosis Table 5 FIGURE 10. with a peripheral distribution. bronchiectasis. This particular distribution pattern can be very helpful in narrowing the differential diagnosis. Bronchiolitis obliterans organizing pneumonia (BOOP) is a disease characterized histologically by the presence of granulation tissue plugs within respiratory bronchioles and alveolar ducts. Bronchiolitis obliterans organizing pneumonia.0 mm collimation) shows bilateral patchy areas of GGO in both a bronchovascular and peripheral distribution. usually adjacent to areas of consolidation. The CT scan appearance of lung contusion is that of ill-defined areas of GGO.33 Desquamative interstitial pneumonitis is characterized by alveolar filling with macrophages.

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