The pericardium is something of a mystery. As the vermiform appendix, we can live well do without it, yet when it becomes sicked it can, because of its strategic position, place a chokehold surround the heart and therefore threaten life itself.
The pericardium is a fibroserous, fluid-filled conical sack that surrounds and encompassing the muscular body of the heart and the roots of the great cardiac vessels as the aorta, pulmonary artery, pulmonary veins, and the superior and inferior vena cavae(1,2) (Fig I).
Under normal circumstances, the pericardium seperates and isolates the heart from contact of the surrounding tissues, allowing freedom of cardiac movement within the restrains of the pericardial space.
This chapter deals with the structure of the pericardium and will give an outline of the embryological development, anatomical structure, innervation, functions and clinical significance of the pericardium.
Embryological Development of Pericardium
Formation of the human body cavities
During the fourth week of gestation, the sides of the embryo begin to grow ventrally generating two lateral body wall folds. These two folds consist of the parietal layer of lateral plate mesoderm, overlying ectoderm, and cells from adjacent somites that migrate into the mesoderm layer across the lateral somitic border(3). As these folds develop, the endoderm layer also folds ventrally and closes to form the gut tube. By the end of the fourth week, the lateral body wall folds meet in the mid-line and fuse to close the ventral body wall. This closure is assisted by growth of the head and tail regions which cause the embryo to curve into the fetal position (Fig. II).
Somatic mesoderm cells cover the intraembryonic cavity transform into mesothelial and become the parietal lining of the serous membranes layers the outside of the peritoneal, pleural, and pericardial cavities.
i. As the head end of the embryo develops forward and folds off from the yolk sac, the 2 compact chains approach each other ventrally and also acquire a lumen lined by endothelial cells. Thus, the 2 endocardial tubes are formed.
ii. The lumen of each of the 2 tubes slowly expands cranially into the midline cell strands and finally the 2 meet.
iii. With another lateral folding of the embryo, the fusion of the 2 endocardial tubes then develops from the cephalic point in a caudal focus, thus forming a single endocardial tube(3,4).
At the same time, with lateral folding and the medial migration and fusion of the tubes, the intracoelomic cavities, right and left, also approach each other in the midline. Ab inito, at the 4 somite state which occurs around day 21, the primitive heart tubes are attached to the anterior and posterior walls, between the right and left coelomic cavities, by the dorsal and ventral mesocardium.
i. While the ventral part vanishes just after its early formation, the dorsal mesocardium remains a little longer.
ii. Whereas the heart tube elongates, curves, and loops, it gradually submerges into the dorsal wall of the pericardial cavity, which is formed from a fusion of the right and left intraembryonic coelomic cavities.
iii. Finally, beginning at the cranial end, the dorsal mesocardium also breaks down and has completely disappeared at the 16-somite stage; and the heart tube is then freely holded up in the pericardial cavity and is connected to the surrounding tissues only at its cephalic and caudal ends(3). The newly developed channel, dorsal to the primitive heart tube, is the futurity of transverse sinus of the pericardial cavity. (Figure III).
In week 5, the intraembryonic coelom comprises of a thoracic and abdominal parts, linked by a canal found on each side of the foregut. In the adult, the intraembryonic coelom is splitted into 3 well-defined compartments: the pericardial cavity with the heart, the pleural cavities with the lungs, and the peritoneal cavity with the viscera below the diaphragm. The diaphragm forms the septum transversum between the thorax and abdomen; the pleuropericardial membrane forms between the pericardial and pleural cavities.
The septum transversum is a thick plate of mesodermal tissue occupying the space between the thoracic cavity and the stem of the yolk sac (Fig II and III). This septum does not divide the thoracic and abdominal cavities entirely but remains large openings, the pericardioperitoneal canals, on each side of the foregut.
When lung buds start to grow, they enlarge caudolaterally within the pericardioperitoneal canals. As a result of the rapid development of the lungs, the pericardioperitoneal canals become too small, and the lungs begin to expand into the mesenchyme of the body wall dorsally, laterally, and ventrally and lateral expansion is posterior to the pleuropericardial folds. With expansion of the lungs, mesoderm of the body wall divides into two parts (4,5) (Figure IV); the final wall of the thorax and the pleuropericardial membranes, which are extensions of the pleuropericardial creases that consist the common phrenic nerves and cardinal veins. Subsequently, they merge with each other and with the base of the lungs, and the thoracic cavity is splitted up into the final pericardial cavity and two pleural cavities. The pleuropericardial membranes constitute the fibrous pericardium in the adult.
Congenital defects of the pericardium are rare(5). Total absence of the pericardium is rarely symptomatic. Usually, the congenital pericardial failure is not recognize until surgical exploration or postmortem investigation is conducted. Yakut et al(6) have reported the pathology of two patients who were operated for other cardiac disease and diagnosed with complete congenital pericardial agenesis.
Anatomical Structure of Pericardium
In humans, the 1 to 3mm thick fibrous pericardium develops a flask-shaped bag. The pericardium is a fibroserous membrane that overlies the heart and the root of its great vessels(1,2,7). The neck of the pericardium on superior aspect is closed by its extensions surrounding the great cardiac vessels; the base is attached to the central tendon and to the muscular fibers of the left side of the diaphragm. Great portion of the diaphragmatic connection of the pericardium has loose fibrous tissue that can be easily detached, but there is a small secion over the central tendon where the diaphragm and the pericardium are entirely merged.
Assessment of the pericardium shows that it is consisted of two interconnected different and isolated anatomical structures (Figure V). The outer sac is known as the fibrous pericardium and has fibrous tissue. The inner sac is known as the serous pericardium and is a delicate membrane resting on loose connective tissue that lies within the fibrous pericardium, lining its inner walls. The heart penetrates the wall of the serous sack from above and behind, forming an infold surrounding nearly the whole pericardial cavity(7,8).
The fibrous pericardium(FP) is the outermost layer, and it is firmly bound to the central tendon of the diaphragm. Extrapericardial adipose tissue, is usually found in the corners between the pericardium and diaphragm on both side, and can be identifiable radiographically(9). The FP defends the heart against brist overfilling since it is persistent and nearly associated to the great vessels that penetrate it superiorly. The pericardium is connected to the sternum by the sternopericardial ligaments and is disciple to the mediastinal pleura except where the two are divided by the phrenic nerves.
The fibrous pericardium is originated from connective tissue cells, collagen fibers, small elastic fibers, lymphatics and microvasculature. The epicardial layer is composed of connective tissue as well as neural elements and blood vessels (10). Coarse collagenous bundles in the epipericardial layer compose the sternopericardial ligaments. Mast cells, lymphocytes and histiocytes may be located in each of the fibrosal and epipericardial stratums. The diversed arrangement and the wavelike orientation of the collagen fibers in the fibrous stratum are such that they permit for some degree of multidirectional stretch. However, given the inextensible nature of collagen fibrils, once the collagen fibrils are straightened out, other stretching of the fibrous layer is limited. It has also been shown that the waviness of the pericardial collagen is maximal in young adulthood and decreases thereafter with age (11).
The fibrous pericardium continuous superiorly with the tunica adventitia of the great vessels entering and leaving the heart and with the pretracheal layer of deep cervical fascia. It attached anteriorly to the posterior surface of the sternum by the sternopericardial ligaments, which are highly variable in their development. The FP bound posteriorly by loose connective tissue to structures in the posterior mediastinum and continuous inferiorly with the central tendon of the diaphragm.
The internal layer of the FP is lined with a glistening serous membrane, the parietal layer of serous pericardium(9,11). This surface is mirrored onto the heart at the great vessels “aorta, pulmonary trunk and veins, and superior and inferior venae cavae” as the visceral layer of serous pericardium(Figure V).
The serous pericardium is composed mainly of mesothelium, a single layer of flattened cells forming an epithelium that lines both the internal surface of the fibrous pericardium and the external surface of the heart. Flattened mesothelial cells those luminal layer is entirely lined with surface microvilli and few cilia that are considered to serve as both specialized friction-bearing surfaces also to widen the cell surface area available for fluid transport(10). Histologic examination of the serousal pericardium suggests the capability of the luminal surface to modify its configuration as well as the ability to permit both transport through intercellular spaces and across the cytoplasm by vesicular transport(12).
The potential space between the parietal and visceral layers consists a thin coat of liquid and is known as the pericardial cavity. It normally contains less than 50 ml of serous fluid which in normal hearts is contained in the pericardial recesses and sinuses mostly over the atrioventricular and interventricular grooves that allows the heart to move and beat in a frictionless setting.
The pericardium is affected by motions of the heart and great vessels, diaphragm and the sternum. Between the left pulmonary artery and subjacent pulmonary vein is a triangular crease of the serous pericardium named as the ligament of the left vena cava (rudimentary fold of Marshall). It is made up by a serous stratum over the fragmnet of the lower part of the left superior vena cava (duct of Cuvier), that regresses during fetal life, but persists as a fibrous band stretching from the highest left intercostal vein to the left atrium, where it lines up with a small vein named as the vein of the left atrium (oblique vein of Marshall), ultimately opening into the coronary sinus(13). The inferior wall (floor) of the fibrous pericardial sac is tightly attached and confluent (partially blended) centrally with the central tendon of the diaphragm. The site of continuity has been known as the pericardiacophrenic ligament; which firmly inchor the pericardium and maintain the alignment of the heart within the thorax. Regardless, the FP and central tendon are not two separate structures that merged together secondarily, nor are they separable by dissection. As a result of the attachments just explained, the heart is somewhat well secured in place inside this fibrous sac.
Pericardial Sinuses and Reflections
The visceral stratum(layer) of serous pericardium forms the epicardium, the outmost of three layers of the heart wall. It expands onto the origination of the great vessels, continuous with the parietal layer of serous pericardium. This reflection creates two invaginations one is where the aorta and pulmonary trunk leave the heart and the other where the SVC, IVC, and pulmonary veins enter the heart(9-12).
The transverse pericardial sinus lies between these two groups of vessels and the reflections of serous pericardium around them, and the reflection of the serous pericardium around the second group of vessels defines the oblique pericardial sinus. The pericardial sinuses form during development of the heart as a consequence of the folding of the primordial heart tube. As the heart tube folds, its venous end moves posterosuperiorly (Fig. I) so that the venous end of the tube lies adjacent to the arterial end, separated only by the transverse pericardial sinus, a transversely running passage in the pericardial sac between the origins of the afferent and the efferent great vessels (Figure VI). Thus the transverse sinus is posterior to the intrapericardial parts of the pulmonary trunk and ascending aorta and anterior to the SVC and superior to the atria of the heart. The superior sinus or superior aortic recess extends up on the right portion of the ascending aorta to the beginning of the innominate artery(12). The superior sinus also joins the transverse sinus behind the aorta, and they are both continually fused until they reach the aortic root.
As the veins of the heart develop and expand, a pericardial reflection surrounding them forms the oblique pericardial sinus, a wide pocket-like recess in the pericardial cavity posterior to the base (posterior aspect) of the heart, formed by the left atrium(Fig VI). The oblique sinus is bounded laterally by the pericardial reflections surrounding the pulmonary veins and IVC and posteriorly by the pericardium overlying the anterior aspect of the esophagus. The oblique sinus can be entered inferiorly and will admit several fingers; however, they cannot pass around any of these structures because the sinus is a blind sac(cul-de-sac).
Clinical importance of the transverse pericardial sinus
The transverse pericardial sinus is particularly important to cardiac surgeons(13). After the pericardial sac is opened anteriorly, a finger can be passed through the transverse pericardial sinus posterior to the aorta and pulmonary trunk (Figure VII). By placing a surgical clamp or placing a tying around these vessels, inserting the canulas of a cardiopulmonary bypass machine, and then tightening the tying, surgeons can stop or divert the circulation of blood in these large arteries while conducting cardiac surgery, such as coronary artery bypass grafting(CABG).
Blood Supply and Innervation of The Pericardium
The arterial supply of the pericardium is mainly from a slight branch of the internal thoracic artery, the pericardiacophrenic artery, that often accompanies or at least parallels the phrenic nerve to the diaphragm (Figure VIII). Smaller contributions of blood come from the: musculophrenic artery, a terminal branch of the internal thoracic artery; bronchial, esophageal, and superior phrenic arteries, branches of the thoracic aorta; and coronary arteries (visceral layer of serous pericardium only), the first branches of the aorta(11,14).
The venous drainage of the pericardium is from the: pericardiacophrenic veins, tributaries of the brachiocephalic (or internal thoracic) veins and also there are variable tributaries of the azygos venous system.
The innervation of the pericardium is from the phrenic nerves (C3-C5), primary source of sensory fibers; pain feeling transmitted by these nerves are generally referred to the skin (C3-C5 dermatomes) of the ipsilateral supraclavicular region. There is also affect of vagus nerve on pericardium with undefined function. Lastly, the vasomotor nerve supply of the pericardium is conveyed by sympathetic trunks(1,2).
The innervation of the pericardium by the phrenic nerves (they are somatic not visceral nerves, despite their location) and the course of these somatic nerves between the heart and the lungs make little sense unless the development of the fibrous pericardium is considered. It is split or separated from the developing body wall by the developing pleural cavities, which extend to accommodate the rapidly growing lungs. The lungs develop within the pericardioperitoneal canals that run on both sides of the foregut, connecting the thoracic and abdominal cavities on each side of the septum transversum.
The canals (primordial pleural cavities) are too small to accommodate the rapid growth of the lungs, and they begin to invade the mesenchyme of the body wall posteriorly, laterally, and anteriorly, splitting it into two layers: an outer layer that becomes the definitive thoracic wall (ribs and intercostal muscles) and an inner or deep layer (the pleuropericardial membranes) that contains the phrenic nerves and form the fibrous pericardium (7). Thus the pericardial sac can be a source of pain just as the rib cage or parietal pleura can be, although that pain tends to be referred to dermatomes of the body wall areas from which we more commonly receive sensation.
Functions of the Pericardium
The grade of the pericardium impact on wall movement depend on the proportion of cardiac to pericardial size, loading circumstances, and the level of active and passive filling. The presence of the pericardium physically constrains the heart, often resulting in a depressive hemodynamic influence that limits cardiac output by restraining diastolic ventricular filling (15).
The impact of the pericardium on mechanical measures of cardiac performance are usually not clear until ventricular and atrial filling restrictions are reached, for example altering geometrical and mechanical characteristics through causes such as maximum chamber volumes and elasticity. These issues become more evident as these pericardial restrictions become prolonged (7-9).
In particular cases when the restrictive role of the pericardium extensively increases, such as during ‘cardiac tamponade’, an increased intrapericardial fluid volume may arise in crucial restriction by the pericardium, that then clinically diminishes cardiac performance (8,9,12).
Closing of the pericardial incision next to open cardiac surgery has been suggested to (a)escape possible postoperative complications, (b)decrease the frequency of ventricular hypertrophy, and (c)ease the future potential reoperations by lessen fibrosis. Differences in ventricular performance depend on the presence of the pericardium have been reported following cardiac surgery (2,7).
In summary, the pericardium is a unique structure that surrounds the heart and serves several important physiological functional roles. Removal of the pericardium or increase of fluids within this sac will change hemodynamic performance. Nevertheless, following open heart surgery, usually the pericardium is not sutured or closed; the reason for this is under evaluation.