Anatomically, the pericardium consists of two layers. The visceral pericardium is contiguous with the epicardium and the parietal pericardium is the thicker fibrous sac surrounding the heart. Although it is often the parietal pericardium that is typically referred to as the pericardium, it should be emphasized that most disease states simultaneously involve both the parietal and the visceral pericardia. Normally, there is 5 to 10 mL of normal buffering fluid within the pericardial space. The pericardium encases all four chambers of the heart and extends 1 to 2 cm up the great vessels. The pericardium similarly reflects around the pulmonary veins. The pericardial reflection around the great vessels limits the size of the pericardial space at these junctures. The degree to which the pericardium extends along the vascular structures varies from patient to patient.
The pericardium restrains the four cardiac chambers within a relatively confined volume and space within the thorax. Because of pericardial constraint, the total volume of the four cardiac chambers is limited, and alterations in the volume of one chamber must, by necessity, be reflected in an opposite change in volume of another chamber. This linking of intracardiac volumes is the underlying pathophysiology for development of pulsus paradoxus and other findings seen in cardiac tamponade and pericardial constriction.
Pericardial disease can present as several different clinical scenarios, and for each of these, echocardiography can play a significant role. Pericardial effusions can accumulate in any infectious or inflammatory process involving the pericardium. Most infectious and inflammatory processes involve both layers of the pericardium. Table 10.1 outlines the diseases that can affect the pericardium. Acute pericarditis of any etiology may result in accumulation of variable amounts of pericardial fluid. In its early phases, inflammation may be present in the absence of any significant accumulation of pericardial fluid. It is important to evaluate left ventricular function in patients presenting with suspected acute pericarditis to exclude a component of myocarditis.
Because the pericardial space is limited in size, accumulation of significant pericardial fluid reduces the total volume that the four cardiac chambers can contain and may result in hemodynamic deterioration related to effective underfilling of the ventricles. It should be recognized that hemodynamic compromise is related to elevated intrapericardial pressure, which in turn is related to the volume of pericardial fluid and the compliance or distensibility of the pericardium. As such, a slowly developing large effusion may be associated with less hemodynamic compromise than a smaller but more rapidly developing effusion. Acute inflammatory processes of the pericardium typically result in pain and fluid accumulation and more chronically can result in fibrous stranding and stiffening of the pericardium. Thickening of the pericardium eventually can lead to pericardial constriction. Other types of pericardial pathology, such as pericardial cysts and congenital absence of the pericardium, are often noted as incidental findings in asymptomatic individuals or may be associated with atypical and highly variable symptomatology.
Echocardiographic Evaluation of the Pericardium
Detection of pericardial disease was one of the first clinical utilizations of echocardiography. It remains a mainstay in the diagnosis of virtually all forms of pericardial disease and plays an appropriate and valuable role in management of patients with known or suspected pericardial disease (Table 10.2).
Anatomically, the pericardium can be evaluated with Mmode, two-dimensional, and three-dimensional echocardiography as well as intracardiac ultrasound. Normally, there may be a very small amount of fluid in the pericardial space that typically collects in the dependent areas. It is most often appreciated as a very small echo-free space in the posterior atrioventricular groove. This space may increase in size during systole (Fig. 10.1). In the absence of a pericardial effusion, dramatic thickening, or calcification, it is unusual to directly visualize the pericardium with either M-mode or two-dimensional echocardiography. Intracardiac ultrasound has been used to directly visualize the pericardium but is infrequently used for this purpose in clinical practice.
Spread from contiguous infection (e.g., pneumonia)
Fungal
Inflammatory
Associated with connective tissue disease
Rheumatoid arthritis
Systemic lupus erythematosis
Other
Post-myocardial infarction
Acute after transmural infarct
Partial/complete free-wall rupture
Delayed, “Dressler syndrome”
Associated with systemic disease
Uremia
Hypothyroidism
Cirrhosis
Amyloidosis
Malignancy
Direct tumor involvement
Effusion due to lymphatic obstruction
Miscellaneous
Posttrauma
Postsurgical
Radiation induced
Congestive heart failure
Severe pulmonary hypertension
Right heart failure
Down syndrome
Pregnancy
a Many cases of “idiopathic” pericarditis are probably viral or postviral in origin.
Table 10.2 Appropriateness Criteria for Use of Echocardiography in Known or Suspected Pericardial Disease
Indication
Appropriateness
Score (1-9)
1.
Symptoms potentially due to suspected cardiac etiology, including but not limited to dyspnea, shortness of breath, lightheadedness, syncope, TIA, cerebrovascular events
A (9)
11.
Evaluation of hypotension or hemodynamic instability of uncertain or suspected cardiac etiology
A (9)
13.
Evaluation of suspected complication of myocardial ischemia/infarction, including but not limited to acute MR, hypoxemia, abnormal chest X-ray, VSD, free-wall rupture/tamponade, shock, right ventricular involvement, heart failure, or thrombus
A (9)
36.
Evaluation of pericardial conditions including but not limited to pericardial mass, effusion, constrictive pericarditis, effusive-constrictive conditions, patients’ post-cardiac surgery, or suspected pericardial tamponade
A (9)
41.
Initial evaluation of known or suspected heart failure (systolic or diastolic)
A (9)
49.
Evaluation of suspected restrictive, infiltrative, or genetic cardiomyopathy
Reprinted with permission of the ACCF from Douglas PS, Khandheria B, Stainback RF, et al. ACCF/ASE/ACEP/ASNC/SCAI/SCCT/SCMR 2007 appropriateness criteria for transthoracic and transesophageal echocardiography. J Am Coll Cardiol 2007;50(2): 187-204.
Detection and Quantitation of Pericardial Fluid
Pericardial effusion can be detected with all the traditionally used echocardiographic techniques. On M-mode echocardiography, pericardial effusion appears as an echo-free space both anterior and posterior to the heart (Fig. 10.1). The size of the echo-free space is directly proportional to the amount of fluid. There are no accurate M-mode techniques for quantifying the absolute volume of pericardial fluid. It should be emphasized that an isolated anterior free space is not specific for pericardial fluid. An anterior echo-free space may be due to mediastinal fat, fibrosis, thymus, or other tissue.
Most often, two-dimensional echocardiography is used to screen for and quantify pericardial effusion. Most echocardiography laboratories visually quantify pericardial effusion as minimal, small, moderate, or large and further characterize it as either free circumferential or loculated. The effusion should also be characterized as to the presence or absence of hemodynamic compromise. On two-dimensional echocardiography, pericardial effusion tends to be most prominent in the more dependent (i.e., posterior in a patient in a supine position) area and frequently appears maximal in the posterior atrioventricular groove (Figs. 10.2, 10.3, 10.4, 10.5 and 10.6). Using additional views including the parasternal short-axis, apical, and subcostal views, the circumferential extent of an effusion can be reliably determined (Figs. 10.6, 10.7, 10.8, 10.9 and 10.10). Figures 10.3, 10.4, 10.5, 10.6, 10.7, 10.8 and 10.9 were recorded in patients with different amounts of pericardial effusion. Note that in Figure 10.7 the circumferential extent of the effusion is confirmed in the short-axis view. This effusion heart is not constrained by an inflammatory component, and the heart moves freely within the pericardial space buffered by the large pericardial effusion. This variable location from beat to beat is the etiology of electric alternans seen on the electrocardiogram.
FIGURE 10.1. M-mode echocardiograms recorded in patients with pericardial effusions. A: Note the echo-free space (arrow) immediately behind the posterior wall of the left ventricle consistent with a small pericardial effusion (PEF). Also note that the space is larger in systole than in diastole. B: The patient has a larger pericardial effusion with respiratory variation in right ventricular size and septal position.
Effusions may be localized or loculated rather than circumferential. This is not uncommon after cardiac surgery or cardiac trauma in which an inflammatory component of the pericardial effusion may result in unequal distribution of fluid in the pericardial space. Figure 10.11 was recorded in an individual with a more laterally localized pericardial effusion, the maximal extent of which is in the area of the lateral wall.
The pericardium reflects around the pulmonary veins which limits the size of a pericardial effusion behind the left atrium. Previous guidelines had suggested that a fluid collection behind the left atrium was more likely to be plural than pericardial. There are numerous exceptions to this rule, and larger pericardial effusions often collect behind the left atrium as well (Figs. 10.5 and 10.9). Additionally, pericardial fluid may collect in the oblique sinus, which is a potential space bordered by the left atrium and great vessels (Fig. 10.12). In this instance, the pericardial fluid may surround the left atrial appendage and the aorta, left atrium, and pulmonary artery and on occasion has been confused for an abscess cavity.
Several schemes have been used for quantitation of the volume of pericardial fluid, none of which have had universal clinical acceptance. Typically, a minimal pericardial effusion represents the normal amount of pericardial fluid in a disease-free state (Fig. 10.2). It is visualized as a small echo-free space in the posterior atrioventricular groove that may be visible only in systole when the heart has pulled away from the pericardium. A small effusion is defined as one resulting in as much as 1 cm of posterior echo-free space, with or without fluid accumulation elsewhere. Smaller effusions tend to collect in the dependent aspect of the pericardial space and, as such, their exact position may vary with patient position. Moderate effusions have been described as 1 to 2 cm of echo-free space and large effusions as more than 2 cm of maximal separation. It should be emphasized that these definitions may vary from laboratory to laboratory. In large effusions, the heart may swing within the pericardial space (Figs. 10.7 and 10.10).
FIGURE 10.2. Parasternal long-axis echocardiogram recorded in a patient with a minimal pericardial effusion. This amount of pericardial fluid represents the normal fluid seen in disease-free individuals. A: Recorded at end-diastole. B: Recorded at end-systole. Note that at end-diastole, there is no separation between the epicardium and the pericardium. At end-systole, the epicardium has lifted off the pericardium revealing a very small pericardial effusion, maximal in the posterior interventricular groove (arrows). DAo, descending aorta.
FIGURE 10.3. Parasternal long-axis echocardiogram recorded in a patient with a small pericardial effusion. Note the echo-free space, maximal in the posterior interventricular groove (arrow) and a smaller anterior echo-free space (downward-pointing arrow). In the real-time image, this pericardial effusion can be seen to be present both in diastole and in systole.
FIGURE 10.4. Parasternal long-axis echocardiograms recorded in patients with a small (A) and moderate to large (B) pericardial effusion. A: There is an approximately 1-cm space between the epicardium and the pericardium (arrow), consistent with a small pericardial effusion. B: A larger pericardial effusion is present both anteriorly and posteriorly (arrows).
Three-dimensional echocardiography may provide a unique imaging perspective on the size and distribution of pericardial effusion but has not been shown to be of incremental clinical benefit (Fig. 10.13). Three-dimensional echocardiography potentially provides an accurate technique for determining pericardial fluid volume and distribution but is limited in its availability. Using this technique, the three-dimensional volume of the entire pericardial space can be calculated. The overall total volume of the entire heart (all four chambers) is then likewise calculated, and the pericardial fluid volume is calculated as the difference between these two volumes. Three-dimensional echocardiography may be limited for this purpose because of a limited field of view, which may preclude registration of a three-dimensional data set of significant size to encompass the entire pericardial volume in larger effusions. Although probably accurate for determining the volume of pericardial fluid, this technique has had little clinical acceptance because of the limited availability of three-dimensional scanning and the lack of a clinical need for determining precise pericardial volume as opposed to its hemodynamic effect.
FIGURE 10.5. Parasternal long-axis echocardiogram recorded in a patient with a large pericardial effusion, measuring 4 cm in its greatest dimension posteriorly (arrow). In the real-time image, there is evidence of a swinging heart.
FIGURE 10.6. Parasternal long- and short-axis views of the heart in a patient with a circumferential small to moderate pericardial effusion (arrows). Note the effusion posterior to the left ventricle and anterior to the right ventricle and a mobility of the heart within the pericardial space in the real-time image.
FIGURE 10.7. Parasternal short-axis view recorded in a patient with a massive pericardial effusion (2,500 mL drained at the time of pericardiocentesis). Note the free motion of the heart within the pericardial space. Also note the marked left ventricular hypertrophy secondary to hypertensive heart disease. PEF, pericardial effusion.
FIGURE 10.8. Apical four-chamber view recorded in a patient with a moderate, predominantly lateral pericardial effusion (PEF) (arrow). Also note a smaller fluid collection behind the right atrium.
FIGURE 10.9. Subcostal echocardiogram reveals a moderate to large pericardial effusion. Note the effusion surrounding the entire heart, with its greatest dimension lateral to the left ventricular free wall. Fluid is clearly seen surrounding the right atrium and between the pericardium and the right ventricle.
FIGURE 10.10. Apical four-chamber view recorded from a patient with a large pericardial effusion and a swinging heart. A pleural effusion is also present, which allows direct visualization of the pericardial thickness (arrows) (A). A, B: Recorded from different cardiac cycles. Note the marked change in position of the heart within the pericardial space, which can be appreciated as a swinging heart in the real-time image. This variable position within the thorax is the cause of electrical alternans seen on surface electrocardiography.
FIGURE 10.11. Apical four-chamber (A) and parasternal short-axis (B) views recorded in a patient with a small, localized, predominantly lateral pericardial effusion (PEF). This echocardiogram was recorded approximately 2 weeks after open-heart surgery.
FIGURE 10.12. Transesophageal echocardiogram recorded in a patient with a moderate pericardial effusion and evidence of fluid in the oblique sinus. A: Note the echo-free space bounded by the left atrium, aorta, and pulmonary artery (PA). This represents fluid accumulating in the pericardial reflection around the great vessels. B: There is a similar collection of fluid in the pericardial space surrounding the left atrial appendage (LAA). In the real-time image (B), note the excessive motion of the wall of the left atrial appendage within the pericardial fluid in the oblique sinus. On occasion, the wall of the left atrial appendage can assume a masslike appearance and be confused with a pathologic mass.
FIGURE 10.13. Transthoracic real-time three-dimensional imaging in a patient with a moderate pericardial effusion in parasternal long- and short-axis views. Note the circumferential effusion surrounding the left and right ventricles (arrows) and the excellent visualization of the extent of free fluid surrounding the heart.
Direct Visualization of the Pericardium
In disease-free states, the normal pericardium is rarely visualized with any of the traditional echocardiographic modalities. Intravascular and intracardiac ultrasound can potentially visualize the actual thickness of the pericardium but are obviously invasive techniques. In the absence of a pleural effusion, which creates a fluid layer on either side of the pericardium, the exterior portion of the parietal pericardium abuts the normal intrathoracic structures, and, therefore, its thickness and character cannot be separated from the surrounding tissues. When both pericardial and pleural effusions are present, the thickness of the pericardium in that area can be ascertained from the transthoracic approach (Figs. 10.10 and 10.14). In instances of marked fibrosis and calcification, it may be possible to infer substantial pericardial thickening, but actual measurement of pericardial thickness is problematic. In the presence of calcific pericarditis, there may be marked shadowing seen posterior to the pericardium (Fig. 10.15). It should be emphasized that the normal pericardium is a highly reflective structure and that a bright pericardial echo alone should not be used to establish the diagnosis of constrictive pericarditis or of a thickened pericardium.
FIGURE 10.14. Parasternal long-axis echocardiogram recorded in a patient with a small pericardial effusion (PEF) and a larger pleural effusion (Pl). The presence of concurrent pericardial and pleural fluid allows identification of the parietal pericardium. In this instance, the pericardial thickness can be seen to be approximately 2 mm. Note the position of the two fluid collections with respect to the descending thoracic aorta (black arrow).
FIGURE 10.15. Parasternal long-axis echocardiogram recorded in a patient with a partially calcified posterior pericardium (arrows). The posterior pericardium has pathologic echo intensity and appears thickened, although because of reverberation, the actual thickness cannot be reliably determined. The markedly echogenic pericardium has resulted in reverberation artifact, creating a double image of the left ventricular cavity behind the pericardial space, best appreciated in the real-time image.
FIGURE 10.16. Parasternal short-axis view recorded in a patient with a moderate pericardial effusion related to uremic pericarditis. Note the multiple fibrous strains (arrow) in the pericardial space, many of which appear to bridge the parietal and visceral pericardia.
Additionally, in the presence of fluid accumulation, masses and stranding, which occur on either the visceral pericardium or the interior aspect of the parietal pericardium, can be visualized with two-dimensional echocardiography. Detection of stranding implies an inflammatory or possibly hemorrhagic or malignant etiology of the pericardial effusion (Figs. 10.16 and 10.17). It often is seen in uremic or infectious pericarditis due to a bacterial or fungal organism. Masses within the pericardium can be the result of metastatic disease (Fig. 10.18) but are often seen in pericardial effusions due to an inflammatory process as well (Fig. 10.19).
FIGURE 10.17. Subcostal imaging recorded in a patient with a moderate to large loculated effusion predominantly located over the right atrium and right ventricle related to prior cardiac surgery. As in Figure 10.16, note the inflammatory stranding bridging between the visceral and the parietal pericardia and the appearance of multiple loculated fluid collections.
FIGURE 10.18. Parasternal long-axis echocardiogram recorded in a patient with a large malignant pericardial effusion (PEF). Note the nodular densities overlying on the visceral aspect of the pericardium anteriorly (arrow). Of note, similar densities may be seen in nonmalignant processes as well.
Using M-mode echocardiography, an indirect assessment of pericardial anatomy can be made. Typically, the heart lifts off the parietal pericardium in systole. By increasing the damping of the M-mode beam to a point at which the myocardium is no longer visualized, the M-mode echocardiogram will visualize only the relatively denser pericardial echoes. Persistence of a bright pericardial signal with progressive damping has been one of the M-mode signs of pericardial constriction (Fig. 10.20). Computed tomography and cardiac magnetic resonance imaging can play a valuable role in pericardial disease as well. They can detect pericardial fluid and, depending on fluid density, suggest a hemorrhagic etiology. Their primary advantage over echocardiography is for direct visualization of pericardial thickness (Fig. 10.21).
FIGURE 10.19. Apical four-chamber view recorded in a patient with an inflammatory pericardial effusion related to connective tissue disease. Note the free fluid in the pericardial space overlying the apical and lateral wall of the left ventricle (longer arrow) and the nodular density adherent to the visceral pericardium (smaller arrow) which, in this case, was not associated with malignancy.
FIGURE 10.20. M-mode echocardiogram recorded in a patient with constrictive pericarditis and thickened posterior pericardial echoes. To the right of this frame, in the area marked by the black bracket, damping has been increased to suppress the fainter myocardial echoes. Note that the bright pericardial echo has not been suppressed. Also note the flat motion of the posterior wall after the initial rapid posterior motion (arrow) of the endocardium. PW, posterior wall.
Differentiation of Pericardial from Pleural Effusion
A left pleural effusion results in an echo-free space posterior to the heart in a patient in a supine or left lateral position (Figs. 10.10 and 10.14). Pleural effusion can occasionally be confused for pericardial fluid. There are several echocardiographic clues that help distinguish pericardial from pleural fluid. As noted previously, the pericardial reflections surround the pulmonary veins and tend to limit the potential space behind the left atrium. Because of this, fluid appearing exclusively behind the left atrium is more likely to represent pleural than pericardial effusion. One of the more reliable distinguishing features between a pericardial and a pleural effusion is the location of the fluid-filled space with respect to the descending thoracic aorta (Fig. 10.14). The pericardial reflection is typically anterior to the descending thoracic aorta, and, therefore, fluid appearing posterior to the descending thoracic aorta is more likely to be pleural, whereas fluid appearing anterior to the aorta is more likely to be pericardial. These observations apply to differentiating pericardial from pleural fluid in the parasternal views. In the apical four-chamber view, separation of a localized lateral pericardial effusion from a pleural effusion can often be problematic. When both pericardial fluid and pleural fluid are present, one can frequently identify the parietal pericardium, which serves as an excellent anatomic landmark to define the extent of each of the two fluid collections (Fig. 10.10).
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