CT of the Pericardium 14

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CHAPTER 14 / CT OF THE PERICARDIUM 145

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CT of the Pericardium

REINHARD GROELL, MD

INTRODUCTION

Because of its widespread availability and its cost-effective- ness, echocardiography represents the primary method of choice to image the pericardium. However, echocardiography is operator-dependent, and it often fails to detect the entire pericardium. Thus it is limited in the assessment of the severity of pericardial involvement in various diseases affecting the pericardium. Nataf et al. have demonstrated that echocardiography revealed thickened pericardium in only 62% of patients with constrictive pericarditis (1). Additionally, ultrasound can- not penetrate calcifications that occur frequently in patients with constrictive pericarditis.

Magnetic resonance imaging (MRI) has a great potential in differentiating soft tissues of the pericardium and myocardium. In MRI of the heart, image quality strongly depends on the accuracy of cardiac gating. This can be problematic in the presence of arrhythmia, which frequently occurs in patients with pericardial diseases. Flow artifacts may compromise the evaluation of pericardial fluid during the cardiac cycle. More- over, as a result of signal loss, the amount and distribution of pericardial calcifications cannot be determined accurately with MRI.

Fast computed tomography (CT) scanners that enable imaging of the entire pericardium with high temporal and spatial resolution in virtually every patient can overcome some of these limitations with echocardiography and MRI. More than ever, CT plays an important role in the diagnostic workup of pericardial diseases.

The pericardium is frequently involved in myocardial pathologies, and vice versa. Additionally, clinical symptoms of pericardial diseases may mimic those of myocardial pathologies. That is why CT imaging of the pericardium is generally combined with morphologic imaging of the entire heart, and a proper CT imaging protocol should follow these tasks. In our institution, we acquire subsecond, transverse CT sections of the heart during suspended respiration in the supine patient position, preferably using electrocardiogram (ECG) gating.

Usually, a slice thickness of 1.5–3 mm is used, depending on the clinical question and the patient’s capability to hold the breath.

From: Contemporary Cardiology: CT of the Heart:

Principles and Applications

Edited by: U. Joseph Schoepf © Humana Press, Inc., Totowa, NJ

ANATOMY AND FUNCTION

The pericardium is a flask-like sac that surrounds the heart, and the neck of this sac is attached to the root of the great vessels at the base of the heart. The pericardium comprises an outer fibrous layer (the fibrous pericardium) and an inner serous sac (the serous pericardium) (2). The serous pericardium consists of an inner visceral layer (the epicardium), which is intimately applied to the heart and the epicardial fat, and an outer parietal layer, which lines the fibrous pericardium. The visceral layer is reflected from the heart and the root of the great vessels onto the inner surface of the fibrous pericardium.

The pericardial cavity lies between the two layers of the serous pericardium. Under physiological conditions, it contains 20–25 mL of serous fluid; however, the amount of fluid may vary considerably among individuals, particularly in chil- dren and infants (3). This fluid is an ultrafiltrate of plasma, which is produced by the monolayer of mesothelial cells of the serous pericardium. It is drained into the right lymphatic duct and the thoracic duct.

On its outside, the pericardium is connected anteriorly to the sternum, inferiorly to the diaphragm, and posteriorly to the esophagus, the thoracic aorta, and the spine (2,4). The coronary vessels run in the subepicardial space between the epicardium and the myocardium, which is a connective tissue layer containing fat.

The pericardium is considered to prevent the ventricles from extreme distension and to control the mechanics of ventricular contractions (5–7). However, it is known that even with con- genital absence of the entire pericardium, subjects usually do not suffer from significant pathophysiological changes.

On computed tomography studies of the thorax, the normal pericardium appears as a thin band enveloping the heart (Fig. 1A,B). As the pericardium is surrounded by outer mediastinal and inner subepicardial fat, the visualization of the pericardium on CT strongly correlates with the amount of fat. In general, the more fat that is present, the better one can delineate the pericardium on CT; the presence of subepicardial fat is especially important for the depiction of the pericardium. Typi- cally, subepicardial fat is well developed over the right ventricle, but it may be very thin or even invisible over the left ventricle. That is why it is often problematic to delineate the pericardium from the myocardium at the left lateral myocardial wall. The attachments to the sternum, diaphragm, or thoracic spine are rarely visualized, as they often do not represent dis-

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tinct anatomical ligaments but rather ill-defined fibrous strands within the mediastinal fat.

PERICARDIAL SINUSES AND RECESSES

At the serous reflections of the pericardium around the root of the great vessels at the base of the heart, the pericardial cavity forms the pericardial sinuses (8,9). They are not separate com- partments but represent extensions of the pericardial cavity.

The Nomina Anatomica labels them the transverse sinus and the oblique sinus. Where the pericardium extends onto the great vessels, the pericardial cavity proper as well as the sinuses form recesses. Their differentiation is based on topographic land- marks, since there is no histological difference between the layers of the pericardial cavity, the sinuses, and the recesses.

Recesses of the Pericardial Cavity Proper

The right and left pulmonic vein recesses are extensions of the pericardial cavity proper located between the superior and inferior pulmonic veins on both sides. The postcaval recess lies

behind and on the right lateral circumference of the superior vena cava.

Transverse Sinus

The transverse sinus is located above the left atrium and posterior to the ascending aorta and the pulmonary trunk.

Between the ascending aorta and the superior vena cava, it is connected with the pericardial cavity proper. It extends upwards along the ascending aorta, where it forms the superior aortic recess. This superior aortic recess is frequently visible, and it was one of the first recesses described in CT studies of the mediastinum; it can be divided into an anterior, posterior, and right lateral portion (10). The anterior and right lateral portions are directly related to the thymus, the posterior portion to tracheobronchial lymph nodes. On unenhanced CT images and on magnetic resonance imaging studies, the superior aortic recess may also simulate aortic dissection or intramural hematoma (Fig. 2). The left pulmonic recess is located below Fig. 1A,B. The pericardium (arrows) appears as a thin band enveloping the heart.

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the left pulmonary artery and posterolateral to the proximal portion of the right pulmonary artery. The right pulmonic recess lies below the right pulmonary artery and above the left atrium.

Its posterior circumference is directly related to inferior tracheobronchial lymph nodes. The inferior aortic recess is situ- ated between the ascending aorta and the inferior portion of the vena cava superior or the right atrium, respectively. It may extend down to the level of the aortic valve.

Oblique Sinus

The oblique sinus lies behind the left atrium. It is separated from the transverse sinus by a double reflection of the pericardium between the right and left superior pulmonic veins. On CT, the transverse sinus (including the right and left pulmonic recess) is always clearly separated from the oblique sinus (including the posterior pericardial recess) by a fat plane. The upper, right lateral extension of the oblique sinus is named the posterior pericardial recess. It is located behind the distal right pulmonary artery and medial to the bronchus intermedius. The esophagus runs posterior to the oblique sinus, and inferior tracheobronchial lymph nodes are in close proximity to these structures.

In general, pericardial sinuses and recesses are frequently observed on CT studies of the heart. They may be problematic in the differentiation from lymph nodes, esophageal or thymic processes, or vascular abnormalities. The knowledge of their

typical location and appearance helps the radiologist avoid a misdiagnosis of lymphadenopathy and of other mediastinal pathologies. Rarely, pericardial cysts or tumors that can mimic cardiac tumors may develop in these sinuses and recesses (3).

As the pericardial sinuses and recesses represent extensions of the pericardial cavity proper, it is very likely that pericardial fluid might move from one area to another during the cardiac cycle or during respiration (11).

DEVELOPMENTAL ANOMALIES ABSENCE OF THE PERICARDIUM

Congenital absence of the pericardium may be partial or complete, with a prevalence of 0.01% in postmortem studies (12,13). The majority of cases consists of a partial defect of the pericardium located over the left ventricle or left-lateral to the left atrium and left auricle. Partial defects at the right side of the pericardium or at the diaphragmatic parts are much less common, and complete absence of the pericardium is extremely rare. In 30% of the patients, congenital defects of the pericardium may be associated with malformations of the heart such as tetralogy of Fallot, atrial septal defects, or patent ductus arte- riosus, or with congenital pulmonary malformations such as bronchogenic cyst and lung sequestration. In most patients, total absence of the left-sided pericardium does not result in clinical symptoms; the same is true for very small defects.

However, medium-sized defects carry the risk of cardiac herniation and even strangulation, particularly of the left atrial appendage. In our institution we have examined a patient after left-sided pneumectomy and pericardiectomy, whose heart herniated into the left thoracic space, resulting in compression of the great vessels, which resulted in subsequent cardiac failure (Fig. 3). The symptoms resolved after subsequent re-operation with closure of the left-sided pericardial defect. It is also reported that pericardial defects may predispose the heart to pulmonary or mediastinal infections.

Frequently, the left ventricle is not surrounded by excessive fatty tissue, which makes the delineation of the left-sided pericardium difficult even in normal subjects. Thus, defects of the left-sided pericardium are often not directly encountered on CT. More frequently, these defects are recognized indirectly by a shift of the heart to the left or—when the defect is smaller—

by left-lateral prominence or herniation of the left atrium or left atrial appendage.

PERICARDIAL CYSTS AND DIVERTICULA

Pericardial cysts and diverticula are rare clinical entities (12,14,15). They represent well-demarcated fluid collections that blend with the pericardium. Most often they occur in the right cardio-phrenic angle (Fig. 4); alternative locations in the left cardio-phrenic angle or at the base of the heart are extremely uncommon. Usually they remain constant in size, but slow progression has also been described. Rarely, calcifications may be present in the wall of a pericardial cyst. While pericardial cysts represent encapsulated collections of fluid, diverticula are herniations of the pericardial cavity through a defect of the parietal pericardium (Fig. 5). Although pericardial cysts and diverticula may reach a size of several centimeters, they rarely cause clinical problems. Their radiological importance lies in the differentiation against clinically relevant pathologies such Fig. 2. Pericardial sinuses and recesses (arrows) are located at the

pericardial reflections around the root of the great vessels.

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Fig. 4. Pericardial cyst (arrow) represents well-demarcated fluid collection that is typically located in the right cardio-phrenic angle.

Fig. 3. Dislocation of the heart to the left after left-sided pericardiectomy and pneumectomy, resulting in acute postoperative cardiac failure.

The symptoms resolved after surgical repositioning of the heart with fixation of the pericardial defect.

Fig. 5. Pericardial diverticulum (long arrow) with open communication between the diverticulum and the pericardial cavity. Note contrast material in the pericardial cavity proper (short arrows) after transthoracic puncture of the diverticulum and installation of diluted contrast material.

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as diaphragmatic hernias, abscesses, or bronchogenic cysts.

Uncommonly, pericardial cysts and diverticula may be acquired, such as after severe chest trauma or surgery.

On CT, pericardial cysts and diverticula present as water- equivalent, round or oval fluid collections surrounded by a thin wall without significant wall enhancement at the above-men- tioned typical locations.

PERICARDIAL EFFUSION

The etiology of pericardial effusion comprises a variety of clinical entities such as inflammation (e.g., viral, bacterial, or fungal infections); collagenous and autoimmune disorders (e.g., lupus erythematosus); metabolic diseases (e.g., uremia);

tumors; radiation, drug, or toxic reactions; and trauma (16–18).

Within the first days following transmural myocardial infarction, acute hemopericardium and tamponade may occur as a result of cardiac rupture, which is associated with a high mor- tality rate. Subacute cardiac tamponade may occur after even nontransmural myocardial infarction. Postinfarct pericarditis and Dressler’s syndrome may appear from one week to several months after myocardial infarction, but it rarely leads to cardiac tamponade. Chylopericardium is extremely uncommon and mainly occurs after surgical or traumatic tears of the thoracic duct or in association with neoplastic duct stenoses.

While rapid accumulation of 150–250 mL of fluid may lead to cardiac tamponade, much higher volumes can be tolerated without significant hemodynamic disturbances when they col- lect over a longer period of time.

Usually, pericardial effusion is of low density in the range from 0 to 20 Hounsfield Units (HU). When it contains higher amounts of protein, such as in bacterial infections, or when it is hemorrhagic, its density may rise to 50 HU and more. Fig. 6 shows two patients with high-density pericardial effusions resulting from hemopericardium. In inflammation, the pericar- dial layers may show contrast enhancement (16).

PERICARDIAL THICKENING AND CONSTRICTION PERICARDIAL THICKENING

On CT studies, the thickness of the normal pericardium is 1–2 mm when measured at the levels of the great vessels or the cardiac chambers (9,19,20). Inferiorly, near the diaphragmatic portion of the pericardium, it may appear slightly thicker, owing to partial-volume effects and the insertion of fibers for its diaphragmatic attachment.

That is why measurements of pericardial thickness should be performed at more cranial, midventricular levels. Pericar- dial thickening is frequently observed after operation, radiation therapy, or inflammation, and it may occur with or without accompanying effusion and calcifications. On autopsy, regional thickening and calcifications of the pericardium are frequent findings, and in the majority of cases they are not associated with prior symptoms of constriction. Doppman et al. have demonstrated that most thickened pericardia they observed on CT studies of the chest were hemodynamically insignificant (21).

It is important to consider that pericardial thickening alone without clinical symptoms of cardiac constriction does not establish the diagnosis of constrictive pericarditis (22).

PERICARDIAL CONSTRICTION

Pericardial constriction is defined as fibrotic or calcific thickening and scarring of the pericardium, which then loses its compliance and impairs diastolic filling of the cardiac cham- bers (22–24). It also leads to dissociation of intracardiac and intrathoracic pressures during respiration.

Pericardial constriction is a rare but potentially curable clinical entity. Pericardiectomy is the only known treatment. Peri- cardial constriction is most often idiopathic, but it also may occur after surgery, radiation therapy, or inflammation—particularly after tuberculosis, especially in developing countries.

In most patients, pericardial constriction presents with insidi- ous symptoms of venous congestion and is therefore difficult to diagnose and differentiate from other cardiac diseases. In par- ticular, pericardial constriction may mimic restrictive cardi- omyopathy, which is why their differentiation has to rely on imaging studies that allow exact assessment of peri- and myocardial structures.

According to the topographical distribution of pericardial thickening and calcifications, global forms of constriction can be differentiated from partial forms, in which the pericardium is affected over the right or left side of the heart or in the atrio- ventricular grooves (annular constriction) (Fig. 7) (25). In the majority of patients, calcifications are present in the thickened pericardium, and often these calcifications extended into the pericardial reflection zones at the root of the great vessels. It is particularly important to the surgeon to know the extent and the topographic distribution of pericardial fibrosed and calcified plaques, not only to establish the diagnosis but also to determine the optimal approach and sites (sternotomy vs tho- racotomy) for pericardiectomy. Frequently, the calcifications may invade the right- or left-ventricular myocardium (Fig. 8).

CT is able to assess such possible myocardial invasion of pericardial calcifications, which is a high risk factor during pericardiectomy and which is not easily visible to the surgeon during surgery. Exact visualization of the subepicardial fat layer on CT helps the surgeon determine the sites of potential resec- tability with relatively low risks. Occasionally pericardial constriction is accompanied by myocardial fibrosis or atrophy.

Knowledge of such areas of myocardial atrophy and fibrosis is also crucial for the cardiac surgeon, owing to a high risk of intraoperative ventricular aneurysms when the pericardium is resected over segments of myocardial fibrosis and atrophy (25).

Adequate assessment of pericardial calcifications is important in the diagnostic work-up of patients with constrictive pericarditis, since calcifications are considered to be an indepen- dent risk factor concerning pericardiectomy (26). Knowledge of the topographic distribution of calcifications helps surgeons plan and calculate the risks of pericardiectomy. Secondary CT signs of pericardial constriction include dilatation of the superior/inferior vena cava and of the right/left atrium as well as deformity of ventricular or septal contours.

TUMORS OF THE PERICARDIUM

Primary tumors of the pericardium are very rare. Among the primary benign tumors of the pericardium are lymphangioma, hemangioma, lipoma, and teratoma (27). The most frequent

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Fig. 6. (A) Hemopericardium (arrows) with hemorrhagic distension of the superior aortic recess of the pericardium. (B) Hemopericardium (long arrow) resulting from a ruptured ascending aortic aneurysm. Note compression of the right pulmonary artery (small arrows).

primary malignant pericardial tumor is pericardial malignant mesothelioma; other malignant primary tumors include heman- giosarcoma, fibrosarcoma, malignant teratoma, and liposarcoma. Apart from fat-containing tumors like lipoma and liposarcoma, CT usually cannot characterize these tumors; their definitive characterization has to rely on biopsy.

By far the majority of pericardial tumors are secondary neo- plasms (28). The pericardium is frequently involved in hematogeneous or lymphatic dissemination from various extrapericardial malignant tumors, such as malignant lymphoma or melanoma (Fig. 9). In autopsy examinations, pericardial me-

tastases occur frequently in patients with malignancies, and generally more often than usually recognized. The pericardium may also be directly infiltrated from adjacent tumors, such as carci- noma of the lung, breast, or esophagus. Apart from solid compo- nents, malignant tumors of the pericardium are often associated with hemorrhagic pericardial effusion and possible tamponade.

Usually, the amount of effusion does not directly correlate with tumor volumes. Finally, malignancies of the pericardium may invade the myocardium and vice versa. Similar to constrictive pericarditis, infiltration of the myocardium is indicated by nonvisualization of the subepicardial fat space.

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Fig. 7. Global (A) and annular (B) forms of pericardial constriction (arrows). Dilatation of the atria (A,B) and deformity of ventricular and septal contours (B) represent secondary CT signs of constriction. Persistent visualization of a subepicardial fat space (A) indicates potential surgical respectability of calcified plaques.

CONCLUSION

With the advent of CT technologies during the last decade providing high temporal and spatial resolution, CT gained more and more influence in imaging the pericardium. The latest spiral and electron beam CT scanners enable the imaging of the normal pericardium and the most relevant diseases of the pericardium with excellent image quality and almost free of motion artifacts. Although echocardiography still represents the first-line imaging modality in assessing pericardial morphology and pathology, some of the inherent

limitations of echocardiography can be overcome by CT, such as operator dependence, restricted field of view not covering the entire pericardium, or nonpenetration of calcified plaques.

CT is especially important in the examination of patients with constrictive pericarditis, since exact knowledge of the extent and location of fibrosed and calcified plaques is crucial to the cardiac surgeon to determine the optimal sites and the possible risks of pericardiectomy.

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Fig. 8. Myocardial infiltration of calcified plaques (arrow) is frequently encountered in constrictive pericarditis. Surgical attempts to remove such infiltrating plaques are associated with high risks of developing intraoperative ventricular aneurysms.

Fig. 9. Pericardial metastasis (arrow) from malignant lymphoma.

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