Chapter 18 The Pleura

Several imaging modalities are used to observe the pleural space. The most important is chest radiography, which remains the initial examination in the assessment of pleural disease. Other imaging techniques that may be used include computed tomography (CT) and ultrasound. Magnetic resonance imaging (MRI) plays a limited role in the assessment of pleural abnormalities. Positron emission tomography (PET) and integrated PET/CT scanning are increasingly used in the assessment of pleural malignancy.

ANATOMY AND PHYSIOLOGY OF THE PLEURAL SPACE

The pleura consists of a visceral and parietal layer that is composed of a continuous surface epithelium of mesothelial cells and underlying connective tissue. The visceral pleura covers the lungs and interlobar fissures, whereas the parietal pleura lines the ribs, diaphragm, and mediastinum. A double fold of pleura extends from the hilum to the diaphragm to form the inferior pulmonary ligament. There is no communication between the two pleural cavities. The pleural space is a potential space that contains 2 to 10 mL of pleural fluid in the normal individual. The pleura can produce up to 100 mL of fluid in an hour, and the absorption capacity of the pleural surface is approximately 300 mL per hour.

The parietal pleura is supplied by systemic capillary vessels and drains into the right atrium by way of the azygos, hemiazygos, and internal mammary veins. The visceral pleura is supplied by pulmonary arterioles and capillaries and drains mainly into the pulmonary veins. Fluid is usually produced at the level of the parietal pleura and is drained by the visceral pleura. Lymphatics also play a role in the clearance of pleural fluid in health and disease. Lymphatic drainage occurs through the parietal pleural lymphatics and ultimately reaches the thoracic duct. The lymphatic drainage of the pleural space begins within lymphatic stomas located mainly in the mediastinal, intercostal, and diaphragmatic portions of the parietal pleura. They eventually drain into larger lymphatic channels. The visceral subpleural space is in continuity with the interlobular septa of the pulmonary interstitium. Unlike the parietal pleura, there is no communication between lymphatic channels of the visceral pleura and the pleural space. Lymph from the visceral pleura flows centripetally toward the hila.

The main manifestations of disease in the pleura include pleural effusion, pleural thickening (which may or may not be calcified), pleural air (i.e., pneumothorax), and pleural neoplasms. Primary disease of the pleura is rare. Most pleural abnormalities result from disease processes in other organs.

PLEURAL EFFUSIONS

General Considerations and Clinical Features

Pleural effusions occur when the rates of entry and exit for pleural liquid and protein are no longer in equilibrium. Increased pleural fluid may result from one of six mechanisms (Box 18-1):

1. Increase in hydrostatic pressure in the microvascular circulation, for example, in congestive heart failure (CHF)

2. Decrease in osmotic pressure in the microvascular circulation, as seen in patients with hypoalbuminemia and cirrhosis

3. Decrease in pressure in the pleural space, as occurs in atelectasis

4. Increased permeability of the microvascular circulation, as seen in inflammatory and neoplastic processes in the pleura

5. Impaired lymphatic drainage from the pleural space due to blockage of the lymphatic system by tumor or fibrosis

6. Transport of fluid from the peritoneal space by way of diaphragmatic lymphatic vessels or through diaphragmatic defects, as may occur in patients with ascites

Pleural effusions may be transudates or exudates (Box 18-2). Transudates are usually caused by increased capillary hydrostatic pressure or decreased osmotic pressure, as in CHF, hypoalbuminemia, hepatic cirrhosis, and nephrotic syndrome. Management of transudates usually consists of treatment of the underlying cause, such as CHF. Exudates result from inflammatory and neoplastic processes involving the pleura. Other examples include pulmonary infarction and collagen vascular diseases.

Box 18-2 Types of Effusions

The presence of an exudate requires a clinical investigation to determine the cause of the pleural effusion. Exudates are characterized by the following criteria: a pleural fluid protein concentration divided by the serum protein concentration that is greater than 0.5; a pleural fluid lactate dehydrogenase (LDH) level divided by the serum LDH level that is greater than 0.6; or a pleural fluid LDH level greater than two thirds of the upper limit of normal for the serum LDH level.

An exudative effusion with frank pus is referred to as an empyema. Hemothoraces may arise from traumatic laceration of vessels adjacent to the pleura. A pleural fluid hematocrit greater than 50% of the peripheral blood hematocrit establishes the diagnosis. Hemorrhagic effusions may also occur with neoplasms, tuberculosis, and infarction. Rupture or obstruction of major lymphatic channels, such as the thoracic duct, may result in a chylothorax, suggested by the presence of elevated triglyceride and cholesterol levels in the pleural fluid. Pleural effusions may also contain a high proportion of eosinophils. Causes include drug hypersensitivity, pneumonia, and pulmonary infarction. Intra-abdominal abnormalities may lead to pleural effusions such as ascites, benign ovarian fibroma (i.e., Meigs’ syndrome), hydronephrosis, and pancreatitis.

Predominantly left-sided effusions may be caused by pancreatitis, distal thoracic duct obstruction, Dressler’s syndrome, and postpericardiotomy syndrome. Predominantly right-sided effusions occur in proximal thoracic duct obstruction and ascites related to hepatic or ovarian disease and in endometriosis.

The leading causes of pleural effusion in the United States are CHF, pneumonia, malignancy, pulmonary embolism, viral infection, coronary artery bypass surgery, and cirrhosis. CHF and pneumonia account for more episodes of pleural effusion than the remaining five entities combined.

Radiologic Features

Standard Radiography

On an upright chest radiograph, a free pleural effusion demonstrates a meniscus sign, which is a concave, upward-sloping interface with the lung that causes sharp or indistinct blunting of the costophrenic angle (Figs. 18-1 and 18-2). Approximately 200 mL of fluid usually is necessary to blunt the lateral costophrenic angle, although smaller amounts (>75 mL) can produce a meniscus that blunts the posterior costophrenic angle on the lateral view (Fig. 18-3). A lateral decubitus view of the chest is much more sensitive than the upright view in the detection of pleural effusion, and as little as 5 mL of fluid can be demonstrated on decubitus views (Fig. 18-4).

Figure 18-1 The frontal view shows a small pleural effusion on the left that causes blunting of the left costophrenic sulcus, producing a meniscus.

Figure 18-2 A, The frontal view shows a meniscus in the left costophrenic angle. The effusion extends upward along the left lateral chest wall. B, On the lateral view, the fluid extends anteriorly but reaches a higher level posteriorly than anteriorly.

Figure 18-3 A small pleural effusion is seen only on the lateral view. A, On the frontal posteroanterior radiograph, the costophrenic angle on the right is sharp. B, The lateral view shows minimal blunting of the right costophrenic angle (arrow).

Figure 18-4 A, The lateral view shows blunting of the costophrenic angle posteriorly (arrow). B, Left-side-down decubitus radiograph shows fluid layering along the left lateral chest wall (arrows).

In the upright position in the normal individual, a small amount of pleural fluid accumulates in a subpulmonic position. In certain individuals, a large amount of free-flowing pleural fluid may accumulate in this position before spilling into the costophrenic angles. On the frontal view, this produces a characteristic appearance with elevation of the apparent ipsilateral hemidiaphragm, flattening of the medial aspect, and displacement of the peak of the apparent diaphragm laterally. On the left side, this is easy to recognize because of separation of the stomach bubble from the apparent left hemidiaphragm (Fig. 18-5). A massive effusion produces a complete or nearly complete opacification of a hemithorax, with displacement of the mediastinum to the opposite side (Fig. 18-6). This appearance contrasts with complete atelectasis of the lung, in which the shift of the mediastinum is toward the side of the opaque hemithorax. Moderate to large amounts of pleural effusion may be missed on supine radiographs. These effusions layer posteriorly and produce a generalized increase in opacity of the hemithorax, through which the pulmonary vessels can be visualized (Fig. 18-7). There may be blunting of the costophrenic angle, and the fluid occasionally tracks over the apex of the lung, producing an apical cap.

Figure 18-5 Subpulmonic effusion. On the left, there is separation of the apparent hemidiaphragm from the stomach bubble (black arrow). There is also minimal blunting of the lateral costophrenic angle. On the right, a large effusion extends to the major fissure, subtending a lucent area that represents the superior segment of the right lower lobe (white arrow).

Figure 18-6 Massive effusion. There is a mediastinal shift to the opposite side and a completely opaque left hemithorax.

Figure 18-7 Bilateral effusions are seen with the patient in the supine position. Hazy opacification in both hemithoraces is caused by fluid layering posteriorly in the pleural spaces. The pulmonary vessels can be visualized through the fluid. Fluid is present laterally on the left (arrow) and in the minor fissure.

Fluid may occasionally accumulate within fissures, and these accumulations may produce the appearance of a mass or pseudotumor (Fig. 18-8). Differentiation from a mass can be easily made because the fluid is free and shifts on decubitus views.

Figure 18-8 Pseudotumor. Fluid is seen in the upper and lower portions of the major fissure on the right, and it extends into the minor fissure. Fluid in the fissure may have a tapered or spindle-shaped configuration, as demonstrated in the more cephalad collection.

Pleural effusions frequently loculate (Fig. 18-9); i.e., they do not shift freely in the pleural space because of adhesions between the visceral and parietal pleura. Loculation of fluid occurs in exudative effusions, particularly in patients with empyema or hemothorax.

Figure 18-9 Loculated effusion. CT shows a large collection of pleural fluid in an anterior, nondependent location (arrow). A lenticular collection of fluid lateral to the spine displaces the enhancing lung parenchyma of the left lower lobe.

Ultrasound

Ultrasound may be used to detect pleural abnormalities and to differentiate solid pleural masses from pleural effusions. However, ultrasound is most frequently used for severely ill patients and for patients in the intensive care unit because of the ready availability for bedside imaging. Ultrasound is useful for detecting the presence of pleural fluid and as a guide to aspiration.

Pleural fluid collections may be anechoic or echoic, and they may change shape during respiration. Most collections are anechoic (Fig. 18-10) and are delineated by an echogenic line of visceral pleura and lung. Anechoic effusions are usually transudates, whereas effusions that contain septations represent exudates in approximately 80% of cases (Fig. 18-11).

Figure 18-10 Anechoic pleural fluid collection. The sonogram shows a collapsed right lower lobe surrounded by a large pleural effusion.

From McLoud TC, Flower CD: Imaging of the pleura: sonography, CT and MR imaging. AJR Am J Roentgenol 156:1145-1153, 1991.

Figure 18-11 Empyema with multiple loculations. The transonic space is divided into multiple secondary loculations by curvilinear septa.

From McLoud TC, Flower CD: Imaging of the pleura: sonography, CT and MR imaging. AJR Am J Roentgenol 156:1145-1153, 1991.

Computed Tomography

Free-flowing pleural fluid produces a sickle-shaped opacity in the most dependent part of the thorax posteriorly on CT scanning (Fig. 18-12). CT allows very small amounts of pleural fluid to be detected. Loculated fluid collections are seen as lenticular opacities in fixed positions (see Fig. 18-9). CT is of limited value in differentiating transudates from exudates or in the diagnosis of chylous pleural effusions. Although most chylous effusions are indistinguishable from other causes of pleural effusion on CT, low attenuation consistent with fat or a fat-fluid level in the pleural collection is rarely seen. Acute pleural hemorrhage, however, can be identified by the presence of a fluid-fluid level or by increased attenuation of the pleural fluid collection (Fig. 18-13).

Figure 18-12 Contrast-enhanced CT shows bilateral pleural effusions; the right is greater than the left. Both have low attenuation and form sickle-shaped opacities posteriorly.

Figure 18-13 Hemothorax after a stab wound to left chest wall. Many areas of increased attenuation can be seen in the fluid collection (arrow). Notice the area of active extravasation of contrast (arrowhead) due to injury to left intercostal vessel.

Case courtesy of Justin Kung, MD, Beth Israel Deaconess Medical Center, Boston, MA.

Pleural fluid can be distinguished from ascites by several CT features (Box 18-3), including the displaced crus sign, the interface sign, the diaphragm sign, and the bare area sign. If the diaphragmatic crus is displaced away from the spine by an abnormal fluid collection, the fluid is located in the pleural space (Fig. 18-14). The location of ascites is lateral and anterior to the crus. The interface sign describes a sharp interface that can be identified between fluid and the liver or spleen when ascites is present. In cases of ascites, the interface is sharp, whereas in cases of pleural effusion, the interface is ill defined (Fig. 18-15). If the diaphragm is identifiable adjacent to an abnormal fluid collection in the right upper quadrant, the diaphragm sign is probably the most reliable means of differentiating fluid from ascites (Fig. 18-16). The location of the diaphragm is readily visible in patients with ascites but may not be identified in patients with pleural effusions. Pleural effusion is visualized outside the hemidiaphragm, whereas ascites is seen within the hemidiaphragmatic contour. The bare area is the portion of the right lobe of the liver that lacks peritoneal covering. Restriction of peritoneal fluid by the coronary ligaments from that area is another useful distinguishing sign. To differentiate pleural effusions from intra-abdominal fluid collections, all four signs should be assessed in each case. The attempt to differentiate ascites from pleural effusion may have pitfalls. A large pleural effusion, particularly on the left side, may cause inversion of the diaphragm, resulting in the pleural fluid being located centrally rather than peripherally.

Box 18-3 Computed Tomography: Pleural Fluid versus Ascites

Pleural Fluid	Ascites
Displaced crus
Ill-defined interface with liver and spleen	Sharp interface with liver or spleen
Fluid outside diaphragm contour	Fluid inside diaphragm contour
	Fluid excluded from bare area of liver

Figure 18-14 Displaced crus sign. The pleural fluid lies inside the crus of the diaphragm (arrow) and displaces it away from the spine.

From McLoud TC, Flower CD: Imaging of the pleura: sonography, CT and MR imaging. AJR Am J Roentgenol 156:1145-1153, 1991.

Figure 18-15 Interface sign. A hazy, indistinct interface is seen between the pleural effusion and liver laterally (arrows), and ascites can be seen anteriorly.

From McLoud TC, Flower CD: Imaging of the pleura: sonography, CT and MR imaging. AJR Am J Roentgenol 156:1145-1153, 1991.

Figure 18-16 Diaphragm sign. Ascites (A) lies inside the diaphragm (arrows) and produces a sharp interface with the liver. The pleural effusion (E) is visualized outside the diaphragm.

From McLoud TC, Flower CD: Imaging of the pleura: sonography, CT and MR imaging. AJR Am J Roentgenol 156:1145-1153, 1991.

CT is helpful in the assessment and management of loculated pleural effusions (see Fig. 18-9). Accurate localization of loculated collections is useful before drainage. Loculated effusions have a lenticular configuration with smooth margins, and they displace the adjacent parenchyma. This typical appearance for any pleural process is a distinguishing feature that can help differentiate a pleural from parenchymal process.

Magnetic Resonance Imaging

The role of MRI in the evaluation of the pleura is somewhat limited. MRI does provide certain advantages because of its ability to image the thorax directly in the axial, sagittal, and coronal planes. MRI may be slightly superior to CT in the characterization of pleural fluid (Fig. 18-17). Typically, fluid collections in the pleural cavity have a low signal intensity on T1-weighted images and relatively high signal intensity on T2-weighted images because of the water content. It may be possible to differentiate transudates, simple exudates, and exudates with the use of a triple-echo pulse sequence. Complex exudates have greater signal intensity than simple exudates, which are brighter than transudates. Preliminary results also suggest chylothorax may have distinctive findings on MRI, with signal intensity characteristics similar to those of subcutaneous fat. Subacute or chronic hematomas demonstrate typical signal intensity on MRI with a concentric ring sign, consisting of an outer dark rim composed of hemosiderin and bright signal intensity in the center because of the T1 shortening effects of methemoglobin.

Figure 18-17 T1-weighted (A) and T2-weighted (B) MRI of a complex pleural effusion. The pleural fluid (white arrows) abuts the heart. The water content has low signal intensity on T1-weighted images and bright signal intensity on T2-weighted images. There is also a subacute hematoma (black arrows), which on the T2-weighted image has bright internal signal characteristics and a dark concentric ring due to the hemosiderin content. The high signal intensity collection in the major fissure on the T1-weighted image represents fat (i.e., chylous effusion). There is T2 shortening, similar to that of subcutaneous fat.

From McLoud TC, Flower CD: Imaging of the pleura: sonography, CT and MR imaging. AJR Am J Roentgenol 156:1145-1153, 1991.

Positron Emission Tomography

PET and integrated PET/CT are playing an increasing role in the assessment of pleural malignancy, particularly in evaluating patients with non–small cell lung cancer (NSCLC) with suspected metastatic pleural effusions. For the diagnosis of pleural malignancy in patients with NSCLC, PET has reported sensitivities ranging from 92% to 100% and specificities of 67% to 94%. False-positive results may result from pleural infection or pleural inflammation after talc pleurodesis. Because integrated PET/CT scanners can accurately localize areas of increased FDG uptake to dense talc deposits in the pleura, this potential pitfall can be avoided by careful correlation between the CT and PET images.

A negative PET scan result can be useful for confirming the absence of pleural metastatic disease, particularly when the result of thoracentesis is also negative. However, false-negative PET studies may occur in the setting of small-volume pleural effusions.

EMPYEMA

Clinical Features

An empyema is an exudative effusion with pus in the pleural cavity. Several criteria are used for the diagnosis of empyema (Box 18-4): grossly purulent fluid; organisms identified on the basis of Gram stain or culture; a white blood cell count in the pleural fluid greater than 5 × 10⁹ cells/L, and a pH below 7 or glucose level less than 40 mg/mL. The natural progression of an empyema consists of several phases: from an exudative to a fibropurulent phase to an organizing phase that results in the development of a thickened pleura, or fibrin peel. Early diagnosis and treatment is therefore imperative.

Box 18-4 Fluid Characteristics of Empyema

Grossly purulent

Organisms identified by stain or culture

White blood cell count > 5 × 10⁹ cells/L

pH < 7.0

Glucose level < 40 mg/mL

Most empyemas are the result of acute bacterial pneumonias or abscesses, but they may occur after thoracic surgery, as a result of trauma, or occasionally, from hematogenous dissemination from extrapulmonary sites or direct spread through the diaphragm from a subphrenic abscess. Empyemas are frequently associated with a communication from the lung (i.e. bronchopleural fistula), which produces air in the pleural space. Empyemas may drain into the chest wall, producing an empyema necessitans.