Pericardial Disease

"The major function of most organs is readily apparent and requires no deep knowledge of biology or physiology. However, whether or not the pericardium serves an important function or not has been debated over the years and the debate continues." [1].

The pericardium is composed of two layers: the visceral pericardium and the parietal pericardium. The visceral pericardium is a serous membrane composed of mesothelial cells adherent to the epicardium. The parietal pericardium is fibrous and acellular. It contains collagen and elastin fibers. Collagen fibers are wavy when the pericardium is at low stretch. When the pericardium is stretched, the collagen fibers straighten, resulting in increased stiffness of the tissue [2].

The parietal pericardium has ligamentous attachments to the diaphragm and the sternum. Therefore, the pericardium maintains the heart in its normal anatomic position in the chest by its attachment to the sternum. The pericardium provides a barrier against infection and provides lubrication between the parietal and visceral layers [2]. The pericardium is well innervated, including mechano- and chemoreceptors [2]. These nerve endings likely participate in reflexes resulting from irritation of the pericardium, epicardium, or both. An intact pericardium protects against atrial rupture in dogs with mitral insufficiency and myocardial hemorrhage induced by acute right-sided heart failure.

The pericardium also restrains cardiac filling and enhances diastolic ventricular coupling (Fig. 17-1). The force exerted on the surface of the heart by the pericardium can significantly limit filling [3-5]. This effect is mostly important with high filling of the left and right ventricles. Under normal conditions, the contact pressure between the pericardium and the epicardium is 2 to 4 mm Hg [3,4]. With a left ventricular filling pressure of 25 mm Hg, the contact pressure has been estimated at 10 mm Hg [3,4]. By this mechanism, the pericardium prevents cardiac overdistention and helps balance the output of the right and left ventricles. The pericardium contributes to diastolic interaction (transmission of intracavitary filling pressure across the septum) [2,6]. A portion of the right ventricular diastolic pressure is transmitted to the left ventricle across the interventricular septum and contributes to left ventricular end-diastolic pressure. If the cardiac volume increases, the pericardium contributes even more to the diastolic interaction.
Figure 17.1. Pressure-volume relationship of the pericardium.

The pericardium provides a gliding surface to accommodate heart motion. The pericardial cavity is filled with a variable amount of pericardial fluid. The volume of pericardial fluid present in normal dogs ranges from 1 to 15 ml (0.25 ml/kg). This fluid is an ultrafiltrate of serum containing between 1.7 and 3.5 g/dl of protein and having a colloid osmotic pressure approximately 25% that of serum. The pericardial fluid contains phospholipids that serve to lubricate the heart [7,8]. Because the pericardium is noncompliant and has a small reserve volume, intrapericardial pressure rises rapidly when the volume of its contents increases acutely (see Fig.17-1). Chronic stretching of the pericardium results in hypertrophy and augmentation of the pericardial volume.

Congenital Pericardial Disease

Absence of Pericardium and Pericardial Defects

Absence of the pericardium is rare in dogs and cats. It does not precipitate clinical signs and is usually detected only at necropsy. Partial pericardial defects occur and represent a risk for cardiac herniation. Right atrial herniation through partial pericardial defects has been reported in dogs [9,10].

Pericardial Cysts

Pericardial cysts have been described mostly in companion animals less than 3 years of age. Cysts are either unilocular or multilocular masses. On histologic analysis, they are thought to be cystic hematomas because they do not have an epithelial lining. In some cases, cysts were associated with a peritoneopericardial diaphragmatic hernia. In other cases, cysts were on a stalk at the apex of the pericardium. This suggests that pericardial cysts result from entrapment of omentum, falciform ligament, or liver in the pericardium during development [11-14]. Dogs with pericardial cysts may show no clinical signs or may present with signs related to cardiac tamponade.

Acquired Pericardial Diseases

Pericardial Rupture

Traumatic rupture of the pericardium has been reported rarely in dogs [10]. Rupture of the pericardium after trauma (e.g., automobile accident or blunt thoracic trauma) likely occurs more frequently than it is diagnosed because it usually does not cause clinical signs. However, when the pericardium contracts around the herniated heart during healing, a stricture can develop that compresses the vena cava, causing a Budd Chiari syndrome with ascites and hepatomegaly, caval syndrome with swelling of the head and neck, or both.

Pericardial Effusion

Pericardial effusions are categorized by the clinical pathologic characteristics of the fluid. A transudate occurs secondary to congestive heart failure, peritoneopericardial diaphragmatic hernia, hypoalbuminemia, or increased vascular permeability [15-22]. An exudate results from infectious on noninfectious pericarditis [17,23,24]. Acute pericarditis is not associated with pericardial effusion [2]. Pericarditis has been associated with feline cardiomyopathy and feline infectious peritonitis [17,25-28]. Fungal pericarditis is unusual, with the exception of Coccidioides immitis in dogs living in the southwestern United States [17,29]. Renal failure can induce epicarditis and pericardial effusion in dogs [30]. Hemorrhagic pericardial effusion results from trauma, rupture of the left atrium secondary to mitral valve disease, intoxication with an anticoagulant, and neoplasia, or it may be idiopathic [31-38]. Idiopathic pericardial effusion is the most common cause of acute or chronic non-neoplastic hemorrhagic pericardial effusion in the dog [15,16,20,29,37,38]. Neoplasia of the heart, heart base, or pericardium is the second most common cause of hemorrhagic pericardial effusion in dogs. Hemangiosarcoma of the right atrium is the most common neoplasia. This tumor is often multicentric, involving the spleen or liver at the time of pericardial effusion. Chemodectoma is the second most common cardiac tumor and is most commonly seen in brachycephalic dogs. Mesothelioma of the pericardium is another cause of a hemorrhagic pericardial effusion [15,18,20,22,23,27,37,39-43].

Cardiac Tamponade

The pericardium is fairly noncompliant, and pericardial pressure begins to rise after 5 to 60 ml of fluid accumulates within the pericardium (see Fig. 17-1). The capacitance of the pericardium is influenced by the rate of fluid accumulation. Hypertrophy of the pericardium by slow stretching allows augmentation of pericardial volume and rightward shift of the pressure-volume curve of the pericardium. As a result, the pericardium can accumulate a larger volume of fluid before pressure begins to rise. However, beyond a certain point, pressure increases quickly with a small additional increase in volume. When the pericardium is thickened, as is the case with constrictive pericardial disease, a minor increase in volume causes a significant increase in pericardial pressure [44-50].

The compensatory response to a pericardial effusion is an adrenergic stimulation and a parasympathetic withdrawal. It induces tachycardia and increased contractility [2,51]. Patients on beta-blocker therapy may not be able to show this response. Elevation in pericardial pressure increases diastolic pressure within the heart, which in turn reduces stroke volume. High pericardial pressure exerts its main effect on the right heart by impeding diastolic filling. The effect on the left side is secondary to decreased pulmonary venous return [51-55]. Because part of the vena cava is in the pericardial sac, increased pericardial pressure will directly affect blood flow in the vena cava. Pericardial pressure first equilibrates with right ventricular filling pressure (right-sided heart tamponade) and then with left ventricular filling pressure (left-sided heart tamponade). Right- and left-sided atrial and ventricular diastolic pressures raise and equilibrate at a pressure equivalent to the pressure in the pericardial sac (between 15 and 20 mm Hg). Cardiac output is significantly compromised and systemic venous pressure is elevated [36,44-47,49,50]. The small end-diastolic volume accounts for the small stroke volume. Compensatory mechanisms induce an augmentation in contractility, and a reduction of end-systolic volume, but not enough to normalize the stroke volume. Tachycardia is common as a reflex to maintain cardiac output. Also during cardiac tamponade, the flow of blood from the right atrium to the right ventricle is significantly reduced. Therefore, the y descent on the central venous pressure tracing is absent. Y descent is observed when the tricuspid valve opens. At this time no blood is leaving the heart, and because the right ventricle is fixed with a small volume, the y descent is lost. During cardiac tamponade, a transfer of blood volume occurs into the systemic circulation, resulting in a reduction of the pulmonary vascularity on thoracic radiographs [56].

Decreased cardiac output results in activation of the renin-angiotensin-aldosterone system, causing retention of sodium and water. Activation of the sympathetic nervous system results in positive inotropic and chronotropic effects and vasoconstriction. Atrial natriuretic factor is not increased during cardiac tamponade to counteract the above effects because the atrium is still supported by the pericardium, which limits its dilation. As a result, cardiac tamponade is associated with increases in systemic venous and portal pressures, causing jugular distention and fluid transudation from systemic capillary beds to produce peripheral edema, liver congestion, and ascites [36,44-47,49,50].

Arterial pressures may vary paradoxically with respiration during severe cardiac tamponade. During inspiration, pericardial pressure and right ventricular pressure decrease. Venous return to the right atrium and ventricle are increased. However, because the volume is limited by the pericardium, there is a leftward shift of the septum. Left ventricular end-diastolic volume is decreased, resulting in a reduction of cardiac output and arterial pressure during inspiration. This phenomenon, known as pulsus paradoxicus, is not a pathognomonic sign of cardiac tamponade. It can also occur with obstructive lung disease, restrictive cardiomyopathy, or hypovolemic shock [36,44-47,49,50].

Constrictive Pericarditis

Constrictive pericarditis compromises cardiac filling by causing a non-distensible, thickened, and fibrotic pericardium. This condition has been reported in dogs aged from 3 to 10 years old [57-59].

Chronic pericarditis resulting from any etiology can cause constrictive pericarditis. Chronic idiopathic pericardial effusion, neoplasia, foreign material (e.g., bullets), and infection (coccidiomycosis) are most commonly reported in cases with constrictive pericarditis [58,59]. In most cases, the parietal pericardium is more severely affected than the visceral pericardium. The parietal pericardium can be up to 8 mm thick. In some cases, the visceral and parietal pericardia are both affected, with severe adhesions between them. Pericardial fluid may be present, and if so, the condition is called effusive-constrictive pericarditis. Mesothelial proliferation, inflammation, and fibrosis are common findings on histopathology [58-60].

Constrictive pericarditis affects late diastole. Early ventricular filling is normal and proceeds rapidly until the limit of pericardial distendibility is reached. The thickened, non-compliant pericardium abruptly limits ventricular filling in mid to late diastole. The atrial and ventricular pressure tracings classically show a rapid y descent followed by an abrupt rise to an elevated diastolic plateau. This is referred as the "square root sign" and is considered diagnostic for pericardial constriction (Fig. 17-2). If a small amount of pericardial fluid is present, the rapid y descent is absent.

Figure 17.2. Constrictive pericarditis. Right ventricular pressure tracing showing the "square root sign" and an elevated end-diastolic pressure (8 mm Hg).

Pulmonary capillary wedge pressure, right ventricular diastolic pressures, right atrial, and left ventricular diastolic pressures are all elevated and equal with constrictive pericarditis. If localized fibrosis is affecting one cardiac chamber more than another, this hemodynamic occurrence may not be found. Also, if the patient is volume contracted from diuretics or other causes, volume loading with a crystalloid solution might be required to demonstrate these classic hemodynamic changes. As the condition worsens, cardiac output declines. Central venous pressure does not decrease during inspiration as normal because negative intrathoracic pressure during inspiration is not transmitted to the cardiac chambers. Changes of intrathoracic pressure are still transmitted to the pulmonary vasculature during respiration. During inspiration, the pressure gradient between the left atrium and the pulmonary circulation is reduced, resulting in less left atrial and ventricular filling. It results in an augmentation of right ventricular filling and deviation of the septum toward the left ventricle. The opposite occurs during expiration [2,54]. Augmentation of systemic venous pressure during inspiration with constrictive pericarditis is referred to as Kussmaul's sign.2,60 High central venous pressure and reduced cardiac output result in compensatory retention of sodium and water by the kidney. Inhibition of the atrial natriuretic peptide (atrium cannot dilate) also contributes to the sodium retention. It further exacerbates increases in systemic, central venous, and left-sided filling pressures.