11 Pericardial Disease Jan Bogaert, Andrew M. Taylor,

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11 Pericardial Disease

Jan Bogaert, Andrew M. Taylor, and Steven Dymarkowski

J. Bogaert MD, PhD; S. Dymarkowski MD, PhD

Department of Radiology, Gasthuisberg University Hospital, Catholic University of Leuven, 3000 Leuven, Belgium A.M. Taylor, MD, MRCP, FRCR

Cardiothoracic Unit, Institute of Child Health and Great Ormond Street Hospital for Children, London, WC1N 3JH, UK

CONTENTS

11.1 Introduction 285

11.2 Pericardial Anatomy and Physiology 285 11.3 MRI Techniques 286

11.4 Normal Pericardium 288 11.5 Congenital Anomalies 289 11.5.1 Pericardial Cyst 289 11.5.2 Pericardial Defect 290 11.5.3 Pericardial Diverticulum 290 11.6 Acquired Diseases 291

11.6.1 Effusive Pericardial Disease 291 11.6.2 Pericardial Inflammation 292 11.6.3 Constrictive Pericarditis 294 11.6.3.1 Morphological Abnormalities in Constrictive Pericarditis 295

11.6.3.2 Functional and Haemodynamic Abnormalities in Constrictive Pericarditis 298

11.6.4 Pericardial Masses 301 11.7 Key Points 302 References 302

11.1

Introduction

With the advent of modern non-invasive cardiac imaging modalities such as echocardiography, cardiac computed tomography (CT) and cardiac magnetic resonance imaging (MRI), direct visualization of the pericardium and related pathology has become a reality. Although echocardiography is still the first- line modality used to explore the pericardium, imaging of the pericardium is often suboptimal especially in “non-echogenic” patients such as patients with lung emphysema or chest wall deformities.

Moreover, differentiation between the pericardium

and adjacent pleural fluid, and between paracardiac fat and fluid is often not feasible. Computed tomography and MRI are second-line imaging modalities that have the ability to overcome, by and large, the limitations of echocardiography. Both are tomographic techniques with excellent spatial and contrast resolution. Since the pericardium, a fibro- fluid structure, is surrounded on both sides by fat (mediastinal and epicardial fat layer), excellent contrast is created, and thus the pericardium is a priori ideally suited for evaluation on CT and MRI (Smith et al. 2001). On routine chest CT examinations, the pericardium and pericardial pathology (fluid, inflammation, calcification or masses) are very well depicted. The coupling of CT data acquisition with ECG gating enables reduction in cardiac-related motion artefacts and optimal visualization of the pericardium.

However, the study of the pericardium goes beyond morphological imaging and includes assessment of the impact of pericardial pathology on cardiac function, mainly diastolic heart function and cardiac filling. Often, the severity of pericardial abnormalities is not closely linked to the severity of the patient‘s symptoms and vice versa. Hence, as a rule of thumb, the morphological and functional pa- rameters should be assessed together. MRI is ideally suited to this role, since accurate information can be obtained not only on the pericardial morphology, but also on cardiac function (Francone et al. 2004).

This chapter focuses on MRI of the pericardium and the pathologies that affect the pericardium and presents an MRI approach for assessing patients with suspected pericardial disease using the current arsenal of MRI techniques.

11.2

Pericardial Anatomy and Physiology

The pericardium is a relatively inelastic, thin, flask- shaped sac (Fig. 11.1) that envelops the heart, extends

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to the origin of the great vessels and is attached to the sternum, the dorsal spine and the diaphragm (Hoit 1990). It is composed of two layers, an inner serous membrane consisting of a monolayer of me- sothelial cells and an outer fibrocollagenous layer.

The inner serosal layer, termed the visceral pericardium, is closely attached to the epicardial surface of the heart and covers a subepicardial layer of con- junctive tissue containing fat and coronary vessels.

The serosal layer reflects back on itself to become the inner lining of the outer fibrous layer. Together, these layers form the parietal pericardium.

Besides the pericardial sac, the pericardium contains two major pericardial sinuses which are composed of different recesses (Groell et al. 1999). The transverse sinus is the connection between the two tubes of pericardium that envelop the great vessels (Fig. 11.2). The aorta and pulmonary artery are enclosed in one anterosuperior tube, and the vena cava and pulmonary veins are enclosed in a more posterior tube. Pericardial effusion located in the superior recess should not be mistaken for an intimal flap of an aortic dissection. The oblique sinus lies behind the left atrium so that the posterior wall of the left atrium is actually separated from the pericardial space (Fig. 11.3). This explains why a posterior pericardial effusion is seen behind the left atrium only when it is very large.

The pericardial virtual cavity normally contains between 10 and 50 ml of an ultrafiltrate of plasma (Roberts and Spray 1976). The fluid is produced by the visceral pericardium and drainage of the cavity is towards both the thoracic duct and the right lym- phatic duct.

It is important to emphasize the essential role of the pericardium in maintaining normal cardiac function. An extensive description of all its functions is beyond the scope of this chapter, but, to summarize, the function of the pericardium is threefold: (a) me- chanical function – improvement of cardiac efficiency, (b) membranous function – reduction of friction from cardiac motion, and (c) ligamentous function – limita- tion of cardiac displacement (Spodick 1997). The pericardial sac has a subatmospheric pressure and should be regarded as a compartment between the pleural space and heart chambers. There is a physiological interaction between the pleural space and pericardium, and between the pericardium and ventricles. The latter interaction is more pronounced for the right ventricle (RV) than the left ventricle (LV), because of the thin anterior RV wall. The myocardial transmural pressure is the difference between the pressure in the ventricular cavity and the pericardial pressure, measuring

±3 mmHg at end diastole, and should be regarded as a measure of preload because it expresses the true filling pressure. The pericardium, furthermore, is involved in the interaction between left and right ventricular func- tion, a phenomenon called ventricular dependence or coupling. This phenomenon is explained in the section on constrictive pericarditis (11.6.3).

11.3

MRI Techniques

For many years, the spin-echo (SE)-MRI technique has been advocated for pericardial imaging

Fig. 11.1a-c. Normal pericardium on SE-MRI. T1-weighted fast SE-MRI in the horizontal long-axis (a), short-axis (b), and vertical long-axis (c). The normal pericardium is visible as a thin curvilinear structure (arrows) with low signal intensity surrounded by the bright epicardial and mediastinal fat. Visualization of the pericardium is often hampered along the lateral wall of the LV because of the sparsity of surrounding fat. Parts of the coronary artery tree can be seen in the epicardial fat, such as the right coronary artery (RCA) in Fig. 11.1.b

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Fig. 11.2 a-d. Pericardial recesses on SE-MRI. T1- weighted fast SE-MRI in the transverse plane at four different levels through the origin of the great vessels. Transverse sinus: superior aortic recess, anterior portion (a), posterior portion (b), right lateral portion (c);

transverse sinus: inferior aortic recess (d) and the left pulmonic recess (e).

The oblique sinus (f ) lies behind the left atrium

Fig. 11.3 a-b. Oblique sinus. T1-weighted fast SE-MRI (a) and bal- anced-SSFP cine MRI (b) in the horizontal long- axis plane. The oblique sinus, containing a small amount of pericardial fluid, is visible as a curvi- linear structure (arrows) behind the left atrium (LA). Ao, aorta

(Lanzer et al. 1984). However, currently a variety of MRI sequences are available and should be used to study the pericardium. These sequences can be applied for morphological imaging of the pericardium and other cardiac structures, for the differentiation between pericardial fluid and the pericardial layers, for characterization of this fluid and the layers,

for studying ventricular function and for assessing cardiac filling (Table 11.1). T1-weighted SE-MRI, using a fast, segmented approach, is the preferred sequence for morphological imaging of the heart and pericardium. Use of small fields-of-view and a saturation block on the frontal chest wall may improve the visualization of the pericardium. A va-

a b

c d

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riety of imaging planes can be chosen to image all parts of the pericardium. In practice, imaging can be started with axial views, followed by views in other direction, such as the coronal or cardiac short- axis view. Administration of paramagnetic contrast agents can be recommended in cases of pericardial masses or inflammatory pericarditis. T2-weighted SE-MRI, preferably using a short-tau inversion-recovery (STIR) sequence, is useful for detecting pericardial fluid and/or pericardial inflammation with oedema of the pericardial layers. Furthermore, the contrast-enhanced inversion-recovery MRI technique (CE-IR MRI) with delayed enhancement, a similar MRI sequence to that used for imaging of myocardial infarction (see Chap. 8), can be applied to enhance tissue contrast in the pericardium and thus to better detect pericardial inflammation and oedema (Klein et al. 2003; Bogaert et al. 2004).

Cine MRI, using balanced steady-state free preces- sion (SSFP) gradient-echo sequences, can be used to evaluate both cardiac function and pericardial motion. The assessment of pericardial motion is useful to differentiate normally mobile pericardium from stiffened immobile pericardium in patients with constrictive pericarditis. Real-time MRI can also be used to evaluate the effects of respiration on the ventricular septal motion in patients with clinical suspicion of constrictive pericarditis (see Sect. 11.6.3). MRI tagging can be applied to detect fibrotic adhesion between both pericardial layers (Kojima et al. 1999), and velocity-encoded or phase-encoded MRI (velocity mapping) can be used to study diastolic function by analysing the inflow patterns in the systemic and pulmonary veins and through the atrioventricular valves.

11.4

Normal Pericardium

On SE-MRI, the normal pericardium appears as a low- intensity line that is surrounded by the high-intensity mediastinal and epicardial fat, or medium-intensity myocardium (Sechtem et al. 1986b; Starck et al.

1984; ; Fig. 11.1). In the vicinity of the lung, the pericardium is more difficult to visualize due to the low intensity of the adjacent lung parenchyma. Therefore, the sensitivity of SE-MRI for visualizing the pericardium varies from only 61% for the pericardium over the free wall of the LV to 100% over the region of the RV (Sechtem et al. 1986b). The transverse sinus of the pericardium can be identified in 80% of cases in the transverse or sagittal plane, and in 70% of cases in the coronal plane, and the preaortic and retroaortic recesses of the pericardium in 67–100% of the cases (Im et al. 1988; Fig. 11.2). Similar results have been reported by Groell et al. (1999) using electron-beam CT. Knowledge of the normal anatomy and appearance of the pericardial recesses (especially the superior pericardial recesses) is important in order to avoid misdiagnosis of aortic dissection or confusion with lymph nodes or mediastinal vessels (McMurdo et al. 1985; Solomon et al. 1990; Groell et al. 1999).

Additional cine MRI studies can be very helpful in further differentiating pericardial recesses from the aortic dissection of an enlarged lymph node.

The mean thickness of normal pericardium on SE-MRI varies from 1.2 mm in diastole to 1.7 mm in systole, with similar results reported by Bogaert and Duerinckx (1995) on 2D-coronary MR angiograms. The MRI values are larger than those found in anatomical studies of the heart (0.4–1 mm thickness; see Sect. 4.4.5). The small increase in pericardial thickness during systole is probably related to the volume reduction of the heart during contraction. Although some authors have mentioned an improved visualization of the pericardium during systole (Chako et al. 1995; Sechtem et al. 1986b), images acquired using current fast SE-MRI techniques during breath-holding obtained during mid- diastole provide the best depiction of the pericardium and other structures of the heart. It should be emphasized that perpendicular slices through the pericardium are necessary to obtain reliable mea- surements of the exact pericardial thickness.

It is important to be familiar with the presentation of the normal pericardium on other MRI sequences.

On T2-weighted SE-MRI, the normal pericardium has low signal intensity. On balanced-SSFP (b-SSFP) cine MRI, the pericardial layers have low signal in-

Table 11.1. MRI strategies to evaluate the pericardium

– Pericardial width (normal or increased), position, and extent (focal, multiloculated or diffuse)

– Pericardial delineation (smooth or irregular)

– Signal characteristics (T1- & T2-weighted MRI/gradient- echo; signal void – low, inhomogeneous or high) – Thickness and enhancement pattern of pericardial

layers (SE-MRI/cine MRI/CE-IR MRI)

– Pericardial motion (cine MRI; normal, rigid or immo- bile)

– Ventricular septal shape and motion during early diastolic filling (short-axis view, using real-time cine MRI;

convex to RV, flattened or inverted)

– RV Morphology (normal, compressed or enlarged) – Right atrial and inferior vena caval size (normal or

enlarged) – Pleural fluid

– Inflow patterns (pulmonary/caval veins and atrioven- tricular valves; normal or restrictive physiology)

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tensity, while pericardial fluid has a high signal intensity (Fig. 11.4). However, one should be careful not to overestimate the true pericardial thickness, since chemical-shift artefacts can be present at the fat–fluid interface, creating a low-intensity zone.

On coronary MR angiograms, large portions of the pericardium are visible as intermediately high-signal intensity zones, with thicknesses in the same range as those measured on SE-MRI (Bogaert and Duerinckx 1995). Knowledge of the pericardial appearance on coronary MR angiography is necessary to differentiate pericardium from epicardial coronary arteries. Using the newer 3D coronary MR angiography techniques with balanced gradi- ents, pericardial fluid is visible with a much higher signal than the coronary blood (Giorgi et al. 2002;

Fig. 11.5).

11.5

Congenital Anomalies

11.5.1

Pericardial Cyst

Pericardial cysts (congenital encapsulated cysts) are most frequently found in the cardiophrenic sulcus

(90%), most often located on the right side (70%;

Fig. 11.6). They are implanted on the pericardium and should not communicate with the pericardial cavity. Pericardial cysts are usually found as inci- dental findings on the chest radiograph, visible as well-defined outpouchings on the lateral heart border. On MRI, they appear as a paracardial liquid mass, which may be surrounded by a line of low intensity consistent with pericardium (Sechtem et al. 1986a). The diagnosis of pericardial cysts on MRI is usually easy, because of their location and consis- tency (homogeneous high signal on T2-weighted images). Pericardial cysts are usually asymptomatic, though rarely they may become symptomatic when compressing other cardiac structures (Fig. 11.7).

Pericardial cysts should be differentiated from other cystic structures such as bronchogenic cysts (prefer- entially located around the central bronchial structures, often with a fluid/fluid level) and thymic cysts (located in the upper, anterior mediastinum).

11.5.2

Pericardial Defect

Pericardial defect or agenesis is an uncommon entity and results from an abnormal embryonic devel- opment that may be secondary to abnormalities in

Fig. 11.5a,b. Pericardium and pericardial recesses on 3D- MR coronary angiography.

Tangential view through left coronary artery tree (a), perpendicular view through left main stem and left anterior descending coronary artery (b). Parts of the pericardium and peri- cardial recesses are visible as well-defined high-signal areas (arrows). The signal inten- sity is higher than of the blood in the coronary arteries

a b

Fig. 11.4a,b. Normal pericardium on bal- anced-SSFP cine MRI in cardiac short-axis (a) and vertical long-axis plane (b). The pericar- dial sac is visible as low signal-intensity line while pericardial fluid demonstrates a high- signal (arrows)

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the vascular supply of the pericardium. Pericardial defects occur in a spectrum ranging from a small defect to total absence of the pericardium. They are more common on the left side (70%) than on the right side (4%) or inferiorly (17%) (Amplatz and Moller 1993; Sechtem et al. 1986a). Partial defects (large partial defects more common than small) are far more common than total defects. This congenital abnormality may be associated, in at least one-third of cases, with other malformations, par- ticularly malformations of the heart (tetralogy of Fallot, atrial septal defect, patent ductus arteriosus) or other types of abnormalities (bronchogenic cyst or hiatus hernia; Lorell and Braunwald 1988;

Letanche et al. 1988).

As a consequence of the defect, cardiac structures or portions of the lung can herniate through the defect. The clinical presentation is variable. Patients are often asymptomatic, and the disease is detected on a routine chest radiograph as an abnormal left cardiac contour (Glover et al. 1969). Symptoms occur when cardiac structures are transiently en- trapped or incarcerated in the defect. Herniation of the left atrial appendage through a small defect may lead to infarction of the appendage or the left

coronary artery might be compressed leading to ischemia especially during exercise (Amplatz and Moller 1993).

Contrary to some reports in the literature, the diagnosis of a pericardial defect on MRI is not always straightforward, since in normal conditions the pericardium over the lateral side of the LV is usually not well depicted; corresponding to the most frequent location of pericardial defects (Gutierrez et al. 1985). So, the diagnosis usually relies on other signs such as an abnormal location of cardiac structures. Since herniation is often intermittent in time, positional changes such as positioning the patient in left lateral decubitus position, can be helpful in diagnosing pericardial defects.

11.5.3

Pericardial Diverticulum

Pericardial diverticulum is exceedingly rare, and can be congenital or acquired. This entity cor- responds to a herniation through a defect in the parietal pericardium that communicates with the pericardial cavity (Sechtem et al. 1986a).

Fig. 11.7a,b. Symptomatic pericar- dial cyst. Axial T1-weighted (a) and T2-STIR weighted (b) fast SE-MRI.

A well-delineated homogeneous soft- tissue structure with low signal on T1-weighted and high signal on T2- weighted SE-MRI, corresponding with a pericardial cyst. The pericardial cyst located ventrally to the cardiac apex compresses the left and right ventricle. The cardiac compression can be well appreciated on cine MRI

a b

Fig. 11.6a,b. Pericardial cyst. Axial non-enhanced CT (a) and T1-weighted SE-MRI (b). The pericardial cyst is vis- ible as a well-delineated, homogeneous low-density (0 HU) and low signal-intensity soft-tissue structure visible along the right paracardiac border (arrows), implanted on a normal peri- cardium (arrowhead)

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11.6

Acquired Diseases

11.6.1

Effusive Pericardial Disease

Imaging of pericardial effusions is used to confirm the presence, severity and extent of fluid; to characterize the nature of the pericardial effusion; and to determine the impact of the effusion on cardiac function and filling. Although the diagnosis of pericardial effusion is usually accomplished by echocardiography, the accuracy of echocardiography can be limited in some circumstances: (1) false-positive cases may occur in the presence of atelectasis, or pleural effusion or mediastinal lesions that mimic pericardial effusion; (2) false-negative cases may occur in the presence of loculated fluid collections, such as in cases of inflammatory adhesions or haemopericardium; and (3) there may be difficulties in differentiating fluid from epicardial fat in the anterior or posterior recesses or from pericardial thickening (Walinsky 1978). MRI is of value com- pared with echocardiography because of its ability to better identify anatomical structures and inter- faces, which reduces the false-positive rate. MRI will provide valuable information regarding the distribution of pericardial fluid, which may vary considerably, even though, in 70% of the cases, fluid collection is observed posterolateral to the LV due to the gravitational dependency of the fluid (Sechtem et al. 1986a; Figs. 11 8 and 11.9). Another common location for fluid collection is the superior recess, as witnessed in cases of abundant pericardial effusion.

Although MRI can detect pericardial effusions as small as 30 ml, a relationship between the measured width of the pericardial space and total fluid volume cannot be established because of focal fluid accumu- lations. Regions in which pericardial width is greater than 4 mm can be regarded as abnormal. Moderate effusions (between 100 and 500 ml of fluid) are associated with a greater than 5-mm pericardial space anterior to the RV (Sechtem et al. 1986a). If needed, the exact amount of the pericardial effusion can be quantified by delineating the pericardial sac on con- tiguous slices through the entire heart, similar to the approach used to calculate ventricular volumes or myocardial masses.

Fig 11.8a-c. Small pericardial effusion. T1-weighted fast SE-MRI at three cardiac short-axis levels. The pericardial effusion (arrows) is homogeneously spread within the pericardial sac. Most of the pericardial fluid is located infero-laterally of the right ventricle and supero-laterally of the left ventricle

Fig 11.9. Moderate pericardial effusion using 3D MR coro- nary angiography (balanced-SSFP sequence). The inhomogeneous spread of the pericardial effusion on this short-axis view through the right coronary artery (RCA) is well visible (arrowheads). Most of the fluid (high-signal) in this patient is located along the left side of the heart. The patient has also a small pleural effusion

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Mulvagh et al. (1989) have shown that MRI is more sensitive than echocardiography for the detec- tion of small pericardial effusions; this improved sensitivity is even more pronounced in the presence of loculated effusions when adhesions occur between the visceral and parietal pericardium. In such cases, it is common to observe a heterogeneous and high signal intensity that can be attributed to a reduction of fluid motion and cellular content.

Although a pericardial effusion usually has no or only limited impact on cardiac filling, acute accumulation of pericardial contents (e.g. fluid, blood, air) can lead to a pericardial tamponade with de- creased cardiac filling and impaired stroke volume, a phenomenon that might be lethal within minutes after onset. The symptomatology is linked to the increase in pericardial pressure determined by the absolute volume of fluid, rate of fluid accumulation and the physical characteristics of the pericardium (degree of stretching). The diagnosis of pericardial tamponade is a clinical one that is confirmed by echocardiography. The role of MRI is limited in the acute phase. Hallmarks of cardiac tamponade are:

the diastolic inversion or collapse of the RV free wall (intrapericardial pressure greater than interventricular pressure); right atrial compression during early systole; exaggerated respiratory variation in cardiac inflow; and abnormal flow patterns in the caval veins (Fig. 11.10).

Attempts to characterize the nature of the effusion based on the signal intensity have been disappoint- ing. Pericardial effusions, either transudative or exudative, usually show up on T1-weighted SE-MRI as hypointense owing to the flow-void effects (fluid motion during cardiac contraction). Higher signal intensity might be related to a high proteinaceous or haemorrhagic content. With gradient-echo tech-

niques, especially with the b-SSFP technique, often a better characterization of the pericardial fluid content can be achieved, such as the visualization of fibrinous strands or presence of coagulated blood (Fig. 11.11). Associated abnormalities helpful in the diagnosis are depiction of thickened pericardial blades with assessment of the degree of inflammation (Fig. 11.12; see Sect. 11.6.2).

11.6.2

Pericardial Inflammation

Inflammation of the pericardium (inflammatory pericarditis) can be caused by: infectious diseases (viral/bacterial/tuberculosis/fungal); can be a mani- festation of various systemic diseases (e.g. rheuma- toid arthritis, lupus erythematosus, scleroderma);

can be found in patients with uremia or following an acute myocardial infarction (Fig. 11.13); or can be the result of irradiation (e.g. breast cancer, mediastinal lymphoma). However, often no underlying pathology is found (idiopathic). The symptoms are mainly related to the severity of pericardial inflammation.

In the acute phase, inflammation of the pericardial layers is characterized by formation of young, highly vascularized granulation tissue with fibrin deposition. Usually, a variable amount of pericardial fluid is present, and the fibrin deposition may lead to a fibrinous adhesion of the pericardial layers. Chronic inflammation is characterized by a progressive scle- rosing pericarditis with fibroblasts, collagen and a lesser amount of fibrin deposition. This may progress towards an end-stage, chronic fibrosing pericarditis with fibroblasts and collagen. The main feature of this end stage is a stiff pericardium with constriction of the heart (constrictive pericarditis; see Sect. 11.6.3).

Fig 11.10a,b. Collapse of the right atrial wall (arrowhead) in a patient with pericardial effusion (arrows). Horizontal long-axis view using balanced-SSFP technique.

Collapse of the right atrial wall occurs when the intrapericardial pressure exceeds the right atrial pressure.

Abbreviations: right atrium, RA

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Fig. 11.11a-d. Haemopericardium (ar- rows) 1 week after aortic valve re- placement. T1-weighted SE-MRI in the short-axis (a) and axial plane (c);

balanced-SSFP cine MRI in the short- axis (b) and axial plane (d). In contrast with the high-signal of the bilateral pleural effusion (star), the signal of the pericardial fluid on cine MRI is very inhomogeneous which is highly suggestive for a haemorrhagic content.

Note that the signal of the pericardial fluid on T1-weighted SE-MRI does not allow discrimination between a simple pericardial effusion and a haemopericardium

a b

c d

Fig. 11.12a-c. Chronic inflammatory pericarditis in a patient presenting with pericardial effusion and fever of underdeter- mined origin. On short-axis SE-MRI (a), balanced-SSFP cine MRI (b) a moderate pericardial effusion (star) and thickened pericardial layers (arrows) are clearly seen. On CE-MRI (c), strong enhancement of both thickened pericardial layers is shown, allowing better differentiation between pericardial layers and fluid than on SE-MRI

a b c

Fig. 11.13a-c. Chronic inflammatory pericarditis in a patient with history of proximal occluded left circumflex artery and transmural myocardial infarction. CE-IR MRI in cardiac short-axis shows the infarct as a strongly enhancing thinned lateral LV wall (arrowhead). A diffusely thickened, strongly enhancing pericardium (arrows) is clearly visible with a small pericardial effusion along the left ventricle and inferolaterally of the right ventricle (star)

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Diagnosis of inflammatory pericarditis remains challenging. The thickening of the pericardial layers can be depicted on SE-MRI, and cine MRI (Sechtem et al. 1986a; Fig. 11.14). Presence of an inflammatory component can be best seen on T2-weighted STIR SE-MRI, and after contrast administration using the CE-IR MRI or SE-MRI technique (Fig. 11.15).

Differentiation between pericardial layers and pericardial effusion is achieved using CE-IR MRI or cine MRI (Figs. 11.12–11.15). Pericardial calcifications, which may be associated with chronic fibrosing pericarditis, will appear as focal regions of decreased signal intensity with irregular shapes (Soulen et al.

1985), but are much better demonstrated by CT.

11.6.3

Constrictive Pericarditis

The main hallmark of constrictive pericarditis is a thickened, fibrotic and/or calcified pericardium, constricting the heart and impairing cardiac filling (Myers and Spodick 1999). Today the majority of cases of constrictive pericarditis are late sequelae of viral pericarditis, whereas formerly tuberculous pericarditis accounted for most cases. Other aeti- ologies include infectious pericarditis, connective tissue disease, neoplasm and trauma. Constriction may also be a complication of long-term renal di- alysis, cardiac surgery and radiation therapy. An

Fig. 11.14a-c. Acute relapsing pericarditis. Axial T1-weighted fast SE-MRI before (a) and after (b) adminstration of Gadolinium-dimeglumine, CE-IR MRI (c). An irregular thickened pericardium is found, mainly over the right heart with strong enhancement of the entire pericardium. The CE-IR MRI allows better depiction of the inflammatory thickened pericardium over the left heart than contrast-enhanced SE-MRI

Fig. 11.15a-c. Acute inflammatory pericarditis. Axial T1-weighted fast SE-MRI (a) shows slightly irregular thickening of the pericardium, mainly over the right side of the heart (arrows). On axial T2-weighted STIR fast SE-MRI (b) the pericardium shows hyperintense appearance with cloudy appearance (arrows). Strong enhancement of the pericardium (arrows) on CE- IR MRI (c). On the contrast-enhanced images, only a minimal amount is visible between the inflamed pericardial layers

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often unrecognized (subclinical) acute (viral) pericarditis may evolve into a subacute and later chronic inflammatory pericarditis, leading to progressive pericardial fibrosis and constriction of the heart.

Pathological findings include calcium deposition in a scarred and fibrotic pericardium that is adherent to the myocardium.

A major dilemma in the diagnosis of constrictive pericarditis is that diseases decreasing the myocardial compliance, such as restrictive cardiomyopathy, are also characterized by an impaired ventricular filling and their clinical presentation can be very similar to constrictive pericarditis. Distinction between the two entities is crucial, since constrictive pericarditis is successfully treated by early pericardiectomy while, for restrictive cardiomyopathy, medical treatment is recommended (Kushwaha et al. 1997; Myers and Spodick 1999). The current diagnosis of constrictive pericarditis and differentiation from restrictive cardiomyopathy is based on a combination of: (a) clinical presentation, (b) visualization of pericardial abnormalities and its impact of the other cardiac structures, (c) assessment of cardiac diastolic function and ventricular filling patterns, (d) measurement of cardiac pressures, and (e) less frequently endomyocardial biopsy to rule out specific myocardial disorders (Hancock 2001).

Even with current accurate non-invasive cardiac imaging techniques, the diagnosis of constrictive pericarditis often remains challenging.

11.6.3.1

Morphological Abnormalities in Constrictive Pericarditis

Morphological abnormalities of the pericardium on MRI in constrictive pericarditis are: (a) thickened pericardium, usually with irregular margins, (b) low signal of the thickened pericardium on T1- and T2- weighted SE-MRI due to the presence of extensive fibrosis or calcification (Figs. 11.16 and 11.17). It is commonly accepted that a normal pericardial thickness is 2 mm or less, a thickness greater than 4 mm suggests pericardial constriction, and one greater than 5–6 mm has a high specificity for constriction (Soulen et al. 1985; Spodick 1997). It should be emphasized, however, that the diagnosis of constrictive pericarditis cannot be based on morphological abnormalities of the pericardium alone.

First, other indirect morphological signs associated with constrictive pericarditis may be helpful in the diagnosis of constrictive pericarditis. These are:

(a) narrowing (tubular-shaped) of the ventricles,

(b) narrowing of one or both of the atrioventricular grooves, (c) enlargement of one or both atria, (d) dilatation of the vena cava and hepatic vein, and (e) presence of pleural effusion (Figs. 11.17, 11.18). The ventricular narrowing is usually more pronounced on the right side because of the larger incidence of pericardial thickening over the RV and the thinner right ventricular free wall. The absence of these associated findings, however, does not exclude constrictive pericarditis.

Second, it may be difficult to differentiate a pericardial effusion from constrictive pericarditis on T1-weighted SE-MRI: both pathologies present as a pericardial broadening with low signal intensity. How to differentiate both conditions? (a) A pericardial effusion typically has a signal void (i.e. black signal), while the thickened, fused pericardial blades have a low (grey) signal (Fig. 11.16), except when heavily calcified (Fig. 11.18); (b) the delineation of a pericardial effusion is usually smooth, while irregular in constrictive pericarditis; (c) cine MRI is often useful to differentiate both conditions, since fluid has a high signal intensity on gradient-echo sequences, while thickened pericardium exhibits a low (or very low) signal. Other MRI techniques may be helpful in the differentiation. Kojima et al. (1999) have used MRI tagging to demonstrate fibrotic adhesions between the visceral and parietal pericardial layers. Persistence of the pericardial tag line integrity throughout the cardiac cycle can only occur if there is a fusion of the pericardial layers. To complicate matters, pericardial effusions may be constrictive (effusive-constrictive

Fig. 11.16. Constrictive pericarditis (chronic fibrosing peri- carditis). Transverse SE-MR image. Diffusely thickened, and irregularly defined pericardium surrounding the entire heart (arrows). Note the presence of the left-sided pleural effusion

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Fig. 11.17a-d. Constrictive pericarditis (chronic fibrosing pericarditis) with severe compression of the right ventricle. Transverse T1-weighted SE-MR images (a-c) show a diffusely, and in- homogeneously thickened pericardium surrounding the entire heart (arrows).

Funnel-shaped appearance of the com- pressed right ventricle (star). Presence of bilateral pleural effusion (arrow- heads). Dilatation of the inferior vena cava (not shown). On T2-weighted STIR SE-MRI (d) the thickened peri- cardium has a strongly hypointense appearance (arrows) in contrast with the hyperintense appearance of the pleural effusion

Fig. 11.18 a-f. Calcified constrictive pericarditis. Lateral (a) chest radiograph shows irregular defined, curvilinear pericardial calcifications (arrows). The pericardial calcifications are much better depicted on CT (b). Axial (c, d) and short-axis (d, e) T1-weighted fast SE-MRI show irregular thickened, strongly hypo-intense appearance of the pericardium (arrows). Note the impressive enlargement of the inferior vena cava (IVC), and the slow flow in the left atrium and right atrial appendage

b

d c

a b c

d e f

a

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pericarditis; Sagistra-Sauleda 2004; Sagistra- Sauleda et al. 2004; Fig. 11.19). The inflamed, thickened pericardial layers (with a variable amount of pericardial fluid) may have a constrictive effect on the cardiac filling. While most cases of effusive constrictive pericarditis will eventually evolve to persistent constriction requiring pericardiectomy, some may be transient and resolve spontaneously (transient con- strictive pericarditis; Haley et al. 2004; Fig. 11.20).

CE-IR MRI with delayed imaging may be useful to differentiate between inflammatory and fibrosing forms of constrictive pericarditis (Fig. 11.21; Klein et al. 2003; Bogaert et al. 2004).

Third, except when pericardial calcifications are extensive, MRI is definitely not well suited to differentiate pericardial fibrosis from calcification, be-

cause of a lack in signal intensity difference between both tissues. CT should be considered as the most sensitive technique.

Fourth, pericardial thickening in constrictive pericarditis is often not generalized. This requires a detailed analysis of the entire pericardium, using a combination of different imaging planes (e.g. horizontal long-axis and short-axis images). It is important to understand that focal pericardial thickening, if located at strategic places such as over the atrioventricular grooves, can give raise to a full clinical picture of constrictive pericarditis even when the morphological abnormalities are not that impressive (Fig. 11.22). Less strategically located but otherwise morphologically important pericardial abnormalities can be clinically silent.

Fig. 11.19a,b. Effusive- constrictive form of constrictive pericarditis.

Short-axis SE-MRI (a) and CE-IR MRI (b).

Diffusely thickened pericardium, with strong enhancement of the pericardial layers after contrast administration.

Presence of a small peri- cardial effusion (star) along the inferolateral side of the right ventricle. At surgery, a heavily thickened and inflamed pericardium was found

Fig. 11.20a-c. Transient constrictive pericarditis in a patient with a history of cardiac surgery (replacement of three cardiac valves). After surgery the patient developed pulmonary oedema and cardiac failure. Axial T1-weighted SE-MRI three weeks after cardiac surgery (a, b), and control study 6 months later (c). The first MRI study (a, b) shows an irregularly thickened, hypointense pericardium, mainly over the right heart (arrows) with a straight interventricular septum (arrowhead) and a dilated inferior vena cava (star). Abnormal motion and flattening of the interventricular septum during early diastolic fill- ing. Six months later (c) the pericardial thickness (arrows), ventricular septal shape and motion have normalized.

a b

a b c

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Fifth, the presence of increased pericardial thickness is not an essential feature of constrictive pericarditis. It might even create a diagnostic dilemma in patients with haemodynamic findings suggestive of constriction without increased pericardial thickness. It has recently been shown by Talreja et al.

(2003) that a significant number (up to 18%) of patients with histologically proven constrictive pericarditis have a normal or near-normal pericardial thickness (i.e. less than 2 mm; Talreja et al. 2003;

Fig. 11.23). Pericardiectomy is equally effective in relieving symptoms regardless of the presence or absence of increased thickness. Symptoms in constrictive pericarditis are caused by the stiffness and the degree of constriction, and not by the thickness of the pericardium as such. A pericardium may be extensively thickened but, if not very constrictive, symptoms might be minimal or even absent. On the other hand, a pericardium with a normal or near- normal thickness can be very rigid and, if tightly constricting the cardiac chambers, give rise to a full-blown clinical picture of constrictive pericardi-

tis. In a similar way, the degree of ventricular filling (pre-load) will contribute to the degree of constriction. Assessment of the inflow characteristics and septal motion under fluid challenge (increased preload) sometimes can be helpful in the diagnosis of constrictive pericarditis (see Sect. 11.6.3.2).

11.6.3.2

Functional and Haemodynamic Abnormalities in Constrictive Pericarditis

At least equally important in the diagnosis of constrictive pericarditis is the analysis of the impact of pericardial changes on ventricular function and cardiac filling (the constriction factor). MRI is not able to measure ventricular filling pressures, but can be applied to study the indirect effects of the increase and equalization of ventricular pressures on ventricular filling. This can be done by velocity or phase-encoded MRI, analysis of inflow patterns through the atrioventricular valves and venous return in the caval and pulmonary veins.

Fig. 11.21a,b. Constrictive peri- carditis. Axial T1-weighted SE- MRI (a), and CE-IR MRI (b).

Irregularly thickened pericar- dium (arrows) over the right heart without enhancement after contrast administration (b). On cine MRI, the thickened pericardium is rigid and immobile (not shown). Histology of the pericardiectomy specimen shows chronic fibrosing pericarditis with mainly fibroblasts and collagen

Fig. 11.22 a-b. Focal constrictive pericarditis. Axial T1-weighted SE-MRI (a) and axial cine-MRI (b) show focal pericardial thick- ening (arrow) at the level of the right atrioventricular groove and basal part of the free wall of the right ventricle with focal compression of the heart. The very low signal of the focal pericardial thickening is caused by pericardial calcification. (Partially reprinted from B. Giorgi et al.

Radiology 2003, 228:417-424, with permission.)

a b

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The increased filling pressures lead to an enhancement of early, diastolic filling (pseudonormalization pattern). Depending on the degree of pericardial constriction, ventricular filling in late diastole is impaired, with an abrupt stop in filling once the fixed cardiac volume is reached (Fig. 11.24). As a result, the atrial filling peak is decreased or absent.

Flow analysis of the venous return shows a diminished, absent or even a reversed systolic forward flow due to the increased atrial filling pressure, an increased diastolic forward flow and an increased

atrial backflow (Fig. 11.24). Unfortunately, a very similar pattern is found in patients with restrictive cardiomyopathy. To discriminate both conditions, the influence of respiration on right and left ventricular cardiac filling patterns should be assessed.

In normal conditions, inspiration decreases the in- trathoracic pressure, leading to an enhancement of RV filling (increased systemic venous return) and decreased LV filling (pooling of blood in the pulmonary veins); an opposite phenomenon is found during expiration. In patients with constrictive peri-

Fig. 11.23a-c. Non-thickened constrictive pericarditis in a patient with previous CABG surgery, presenting with increased right heart filling pressures, dyspnea and peripheral oedema. Transthoracic echocardiography shows restrictive physiology.

Axial T1-weighted SE-MRI at three levels through the heart. The pericardium is visible as a thin curvilinear line with a maximal thickness 1.7 mm (arrows). Real-time cine MRI of the ventricular septal motion shows diastolic septal inversion at the onset of inspiration, and an increased total septal excursion (“pathologic ventricular coupling”; see Fig. 11.25). During the pericardiectomy, a non-thickened but very stiff pericardium was found, and the cardiac output increased spectacularly from 1.7 to 7.5 l/min

Fig. 11.24a-d. Inflow curves, using velocity- mapping MRI, through the mitral valve (a), tricuspid valve (b), pulmonary vein (c) and inferior vena cava (d) in a patient with constrictive pericarditis (same patient as in Fig. 11.18).

Inflow curves show a severe restrictive inflow physiology with absent A-waves through the atrioventricular valves (a, b), and absent systo- lic forward in the infe- rior vena cava (d)

a b c

a b

c d

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carditis, this pattern is enhanced owing to the presence of a stiff pericardium, while in patients with restrictive cardiomyopathy this pattern is normal or diminished (Hatle et al. 1989). Although real-time velocity mapping is feasible, accurate assessment of the transvalvular or venous flow patterns might be hampered by problems of through-plane motion caused by the respiration.

Alternatively, analysis of the position and configuration of the interventricular septum with MRI is of interest in patients with clinical suggestion of constrictive pericarditis. The position and configuration of the septum is primarily determined by the transseptal pressure gradient. In the unloaded or unstressed human heart, the septal configuration is flat, while it becomes concave in shape towards the LV, during normal loading conditions owing to a left-to-right positive transseptal pressure gradient.

The phenomenon whereby the function of one ventricle is altered by changes in the filling of the other is called ventricular interdependence or ventricular coupling (Taylor et al. 1967; Janicki and Weber 1980). In patients with constrictive pericarditis, the pericardial inflexibility leads to an increased ventricular interdependence or pathological ventricular coupling, characterized by septal flattening or inversion during early ventricular filling. Since RV filling starts just before LV filling, the presence of a non-compliant pericardium impedes the RV free wall outward motion during filling. As a consequence, the instantaneous diastolic transseptal gradient will change and lead to a septal reconfigura- tion and paradoxical motion during filling. Because of the thin nature of the RV free wall, the influence of pericardial thickening is more pronounced on the right than on the left side of the heart. Moreover, this pattern is typically enhanced by respiration, leading to a pronounced leftward shift during inspiration and an opposite shift during expiration. Besides the physiological effects of respiration on ventricular filling, the thickened, fibrotic pericardium acts as a barrier, creating a pressure gradient between ventricles and supplying veins. This will contribute to the observed septal abnormalities.

In a recent paper by Giorgi et al. (2003) using a breath-hold cine MRI technique, septal flattening during early diastolic filling was found in the majority of patients with constrictive pericarditis.

This pattern was not seen in normal subjects or in patients with restrictive cardiomyopathy or pericardial effusion. The septal abnormalities are typically most evident in the basal part of the interventricular septum. Taking into account the pathophysiology of

abnormal septal motion in constrictive pericarditis, septal flattening may be absent if the constrictive pericardium does not impede the ventricular expansion but restricts the ventricular filling by constricting the atrioventricular groove(s), or when the constrictive pericardium compresses parts of the heart other than the RV (Hasuda et al. 1999).

Moreover, it should be stressed that even in obvi- ous pericardial thickening, septal flattening may be minimal or absent if the ventricular constriction is minimal. However, since the breath-hold acquisition takes several heartbeats, the effects of respiration on cardiac dynamics, an essential feature to differentiate between constrictive pericarditis and restrictive cardiomyopathy, cannot be evaluated. With the advent of real-time MRI techniques, the septal dynamics can be evaluated during free breathing.

The preliminary results from a study by Francone et al. (in press) show in patients with constrictive pericarditis abnormal septal motion with septal flattening/inversion during early ventricular filling. The septal abnormalities are most pronounced in the first heartbeat after the onset of inspiration and rapidly decrease in magnitude during subse- quent heartbeats (Fig. 11.25). During expiration an opposite pattern with increased right-sided septal motion is found. Total respiratory septal excursion, obtained by measuring the maximal distance in septal position between inspiration and expiration divided by the transverse biventricular diameter, is significantly larger in constrictive pericarditis patients (18.7±1.2%) than normal subjects (7.1±2.4 %) and restrictive cardiomyopathy patients (5.8±2.1%).

A cut-off value of 11.9% (mean normal value +2 SD) can be used to discriminate constrictive pericarditis patients from non-constrictive pericarditis patients (see also Chap. 9).

Cine MRI can also be applied to evaluate the motion of the pericardium throughout the cardiac cycle, and thus to get a direct idea about the rigidity of the pericardium. A normal pericardium moves in synchronization with the in- and outward motion of the heart throughout the cardiac cycle, while a fixed pericardium shows a reduced or eventually an absent motion during the cardiac cycle. Moreover, cine MRI allows the demonstration of the restricted ventricular expansion during cardiac filling, abutted towards the thickened, rigid pericardium. Assessment of systolic function is normally also part of an MRI study in patients with constrictive pericarditis. The intrinsic myocardial contractility is normally pre- served (except in cases where the fibrotic/calcified process involves the myocardium or in long-stand-

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ing cases of constrictive pericarditis). As a consequence of impaired ventricular filling, however, stroke volumes and cardiac output are decreased.

11.6.4

Pericardial Masses

Primary tumours of the pericardium are rare entities, occurring much less frequently than pericardial metastasis (see also Chap. 12). The most common primary malignant tumour of the pericardium is the mesothelioma, which is often associated with haemorrhagic pericardial effusion. Other primary tumours include malignant fibrosarcoma, angiosar- coma, and benign and malignant teratoma (Gomes et al. 1987).

Pericardial metastases are relatively common (having a frequency of up to 22% in autopsy series of cancer patients) and are, in most cases, secondary to lung or breast carcinoma, leukaemia or lymphoma (Hanock 1982). They are frequently associated with a large and haemorrhagic effusion that is dispropor- tionate in size to the amount of tumour present. The metastatic pericardial implants are often small and difficult to visualize on MR images.

MRI has advantages over other techniques for the assessment of pericardial tumours, because it better delineates the implantation of the tumour out- lined by either pericardial fat or pericardial fluid, and provides additional information on the contigu- ous anatomical structures (myocardial wall or great vessels). In the assessment of mediastinal and lung tumours, MRI is also the imaging modality of choice

Fig. 11.25. Abnormal respiratory variation of ventricular septal shape and motion in a patient with constrictive pericarditis (“pathologic ventricular coupling”). At the onset of inspiration (1^st heartbeat, hb), a sudden left-sided septal shift with sep- tal inversion is found (arrow). The intensity of septal abnormalities rapidly decreases the next heartbeats. The septum is flattened by the second heartbeat (arrowhead) and becomes convex to the right later during inspiration. During expiration (not shown) the opposite phenomenon is found with increased right-sided septal shift. The respiratory variation in septal position is increased in patients with constrictive pericarditis