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Mechanical properties of human pericardium. Differences in viscoelastic response when compared with canine pericardium.

Whereas most experiments on the mechanical function of the pericardium have been performed on dogs, very little is known about the applicability of those data to humans. To examine the tensile viscoelastic properties of fresh human pericardium, we have used the methods from our previous study of canine pericardium. Although the mechanical responses of canine and human pericardium were qualitatively similar, human pericardium displayed a significantly greater viscous character. Human pericardium was 7.3 times thicker than canine pericardium, but was more extensible in stress-strain tests, with lower stiffness at a given strain. The static (elastic) stiffness of human pericardium seems identical to that of canine pericardium; lower stiffness per unit thickness of the human tissue at predicted physiological stresses was almost exactly compensated by the greater wall thickness. This effect was also seen in data on fracture strength and stiffness. However, human pericardium displayed greater viscous responses than the canine tissue. This was seen in doubled cyclic hysteresis losses, and greater stress relaxation and creep. Our results suggest that experiments on the viscoelastic properties of canine pericardium may not be directly applicable to humans, especially where dynamic mechanical properties are most important: i.e., in studies of ventricular function and the time-course of pericardial effusions.

Adult

Pericardium as a thoracic aortic patch: glutaraldehyde-fixed and fresh autologous pericardium.

The repair of complex coarctation of the aorta often requires an aortic patch. Prosthetic patches lack growth potential and are associated with an increased incidence of aneurysm formation opposite the patch. We compared buffered glutaraldehyde-fixed patches, used in six animals (group 1), and untreated autologous pericardial aortic patches, used in five animals (group 2). Weanling pigs underwent pericardial patch replacement of a 1 X 2-cm diamond-shaped segment of the lateral wall of the descending thoracic aorta at the level of the aortic isthmus. Six months following patch aortoplasty, the animals were killed and the in situ patch dimensions were measured and compared to the measurements obtained at implantation. The increases in length, recorded as mean percentage change +/- SEM, were 34.7 +/- 3.7% for group 1 and 102.8 +/- 20.3% for group 2 animals; the increases in width were 91.4 +/- 31.7% for group 1 and 192.4 +/- 31.4% for group 2. The percentage changes for both length and width were significantly different between groups (P less than 0.05). Pull strength testing of standard-size patch samples demonstrated no significant difference in tensile breaking load between groups: group 1 = 959 +/- 277 g, group 2 = 795 +/- 86 g. Thoracic aortography revealed no evidence of stenosis or aneurysmal dilation in either group. Autologous pericardium is resilient, strong, and readily available and has expansile potential that makes it an ideal aortic patch material. We conclude that glutaraldehyde fixation does not provide additional strength and limits graft expansile potential when compared to untreated pericardium.

Animals

Effects of the pericardium on left ventricular diastolic filling and systolic performance early after cardiac operations.

To determine whether closure of the pericardium after cardiac operations affects the filling characteristics and systolic performance of the left ventricle, we measured left ventricular volume, pressure, cardiac index, and stroke work index in 10 patients between 11 and 15 hours after cardiac operations, with the pericardium first closed and then open. At the time of operation, radiopaque tantalum markers were inserted in the left ventricular myocardium to outline the chamber in the 30-degree right anterior oblique projection, and the pericardium was closed by a continuous polypropylene suture exteriorized at both ends of the sternotomy. The patient was then transferred to the surgical intensive care unit, where left atrial pressure was measured via a fluid-filled catheter, left ventricular pressure with a micromanometer-tipped catheter, and myocardial oxygen consumption via a coronary sinus catheter. Left ventricular volume was measured by computer-aided analysis of fluoroscopic images (recorded at 30 frames per second) of the implanted myocardial markers. Left atrial pressure was maintained at target values of 10, 15, and 20 mm Hg by intravenous augmentation of blood volume. Left ventricular and left atrial pressures and volumes were measured with the pericardium closed; the pericardium was then opened by withdrawal of the pericardial suture. Radiopaque clips on the pericardial edges confirmed opening of the pericardium seconds after withdrawal of the suture. Repeated measurements of left ventricular pressures and volumes were then made at the target left atrial pressures with the pericardium open. End-diastolic volume index, peak positive time derivative of pressure, stroke work index, and cardiac index all increased significantly when the pericardium was opened (p < 0.001). Thus we found the following: (1) At physiologic pressures, the pericardium had a significant constraining effect on diastolic filling of the left ventricle, and (2) opening of the pericardium resulted in increased cardiac index and stroke work index. These increases may be attributed to the Frank-Starling response to increased left ventricular preload. The demonstrated improvement in left ventricular systolic performance should be considered when contemplating closure of the pericardium after cardiac operations, especially in patients with preoperative left ventricular dysfunction.

Adult

Autologous pericardium versus a xenograft substitute in myocardial wound healing.

This study compared repair of myocardial wounds covered with autologous pericardium to healing of wounds covered with glutaraldehyde-preserved bovine pericardium in an experimental canine model. Right (RV) and left (LV) full thickness ventriculotomies were made and closed. In the control group (n = 12), the pericardium was closed over the wound; in the experimental group (n = 12), wounds were covered with bovine pericardium. Animals were sacrificed at 14, 21, 28, and 42 days. After excising the pericardium, 6 mm punch biopsies of normal RV, RV wound, normal LV, and LV wound were assayed for hydroxyproline (HPro). Both autologous and bovine pericardium became densely adherent to the wounds. Bovine pericardium was mildly adherent over unwounded areas, while autologous pericardium was usually free. Normal RV contained more than twice as much HPro as normal LV (5.4 +/- 0.57 micrograms/mg vs 1.7 +/- 0.35 micrograms/mg, P less than 0.0002). A gradual rise in HPro over time was seen in both groups, but this increase was statistically significant only at 42 days (P less than 0.05). There was no significant difference in HPro between wounds covered with autologous pericardium and those covered with bovine grafts (P = 0.13) at any of the sample times in this study. In this experimental canine model, the pericardium does not appear to play a prominent role in myocardial wound healing by contributing collagen-producing fibroblasts. Furthermore, the bovine pericardial xenograft becomes densely adherent to LV and RV incisions. In the clinical setting, such may make reoperation more hazardous when the heart has been previously incised or coronary bypass grafts have been constructed.

Animals

Immunogenicity of glutaraldehyde-tanned bovine pericardium.

Glutaraldehyde-tanned bovine pericardium was tested for its ability to induce immunologic responses in vivo. Sections of glutaraldehyde-tanned bovine pericardium were implanted between the abdominal muscles of rats and guinea pigs. Control animals received Dacron implants. Lymphocytes and sera from animals were isolated at 2 and 4 weeks after implantation (four animals per group per time). Tritiated thymidine incorporation and an enzyme-linked immunosorbent assay were used to measure T- and B-lymphocyte responses to glutaraldehyde-tanned bovine pericardium antigens. At the same time points, implants and surrounding tissue from all animals were processed for histologic data. Results show that T-lymphocytes from animals with glutaraldehyde-tanned bovine pericardium implants responded significantly (p less than 0.001) to glutaraldehyde-tanned bovine pericardium antigens in vitro but not to Dacron. In contrast, lymphocytes from animals with Dacron implants failed to respond to glutaraldehyde-tanned bovine pericardium or Dacron preparations. Results of enzyme-linked immunosorbent assay show that animals with glutaraldehyde-tanned bovine pericardium implants produced antibody directed against glutaraldehyde-tanned bovine pericardium antigens. Histologic study revealed a dense mononuclear and multinuclear giant cell infiltrate at the interface between glutaraldehyde-tanned bovine pericardium and surrounding host tissues, with focal degradation of implant collagen. Dacron elicited a nonspecific lymphocytic and foreign body-type reaction. These results indicate that glutaraldehyde-tanned bovine pericardium can induce immunologic responses in vivo consistent with a host-versus-graft reaction.

Abdominal Muscles

Closure of pericardium after open heart surgery. A way to prevent postoperative cardiac tamponade.

Between July 1968 and December 1975, 821 patients underwent open heart operations. In 596 cases the pericardium was left open and in 225 the pericardium was closed. Forty-one patients in the open pericardium group required reoperation and 23 of these had tamponade. Four patients in the closed pericardium group had reoperation but there was not a single case of tamponade. In most cases that required reoperation the bleeding was from extrapericardial sources. Absence of tamponade in the closed pericardium group can be explained by the fact that blood from extrapericardial sources of bleeding cannot collect round the heart because the pericardium is closed. Thus closure of pericardium helps to prevent tamponade. Reoperations some months or years after the original operation are technically easier and less hazardous if the pericardium has been closed because the closed pericardium prevents the heart from becoming adherent to the back of sternum and also because there are fewer adhesions in the pericardial cavity.

Cardiac Surgical Procedures

[Regional irrigation of the pericardium in children].

PURPOSE: To investigate the irrigation of both fibrous pericardium and the parietal layer of serosal pericardium in children. PATIENTS AND METHODS: The cadavers of 10 children of both sexes, under the age of one. In this study we adopted the regional divisions described by DI Dio, which considers a plane between the two phrenic nerves that divides the areas of pericardium into ventral and dorsal regions. We also refer to these regions as antephrenic and retrophrenic respectively. In addition, we consider the inferior pericardium to be that portion of pericardial sac related to the diaphragm. RESULTS: The pericardium ventralis was more frequently irrigated by branches of the following arteries: thoracicae internae dextra and sinistra, pericardiacophrenica dextra in 9 cases; pericardiacophrenica sinistra in 8 cases; and less frequently, by branches of the arteriae phrenicae inferiores dextra and sinistra, epigastrica superior sinistra, thimica, rami thimici of the a. thoracica interna dextra, and rami thimicus and esophagealis of the a. subclavia dextra. The pericardium dorsalis was more frequently supplied b the following arterial branches: bronchiales in 9 cases; esophagealis of the aorta in 8 cases; and in a frequency inferior than 4 cases, we observed the following arteries: thyroidea inferior sinistra, intercostalis suprema, pericardiacophrenicae dextra and sinistra, subclavia sinistra, coronariae dextra and sinistra, phrenicae superior and inferior sinistra, thoracica interna dextra, intercostales posteriores primae dextra and sinistra, truncus costocervalis and rami esophageales of the a. gastrica sinistra. The pericardium inferior was irrigated by branches of the arteriae phrenicae inferiores dextra in 10 cases and sinistra in 9 cases. CONCLUSION: Analysis of the results demonstrated that similar behavior in the pericardium regional irrigation offers a standard for intervention in the pericardium.

Coronary Circulation

[Morphofunctional characteristics of the hemomicrocirculatory bed of the canine pericardium].

The hemomicrocirculatory bed in the canine pericardium is presented by arterioles, precapillaries, capillaries, postcapillaries and venules situating in various connective tissue layers of the pericardium. Certain morphological peculiarities of the structure of the hemomicrocirculatory bed links are revealed in various parts of the pericardium. As demonstrate morphometry data, the diameter of all the vessels of the hemomicrocirculatory bed in various parts of the pericardium has no precise differences. There are some fluctuations in the number of the capillaries per 1 mm2 in various parts of the pericardium. Their number is comparatively greater in the area of the vascular porta (transitional fold), in the left lateral, in the ventral and dorsal parts of the pericardium. In these parts of the pericardium the density of the capillaries is increased, the network is especially dense in the area where the pericardial transitional fold passes into the epicardium. In the pericardial microcirculatory blood bed adaptive mechanisms (glomeruli, arteriolo-venular anastomoses, microsphincters) performing regulation of the organ's blood stream, are widely presented.

Animals

Prevention of calcification of glutaraldehyde pretreated bovine pericardium through controlled release polymeric implants: studies of Fe3+, Al3+, protamine sulphate and levamisole.

Calcification is the principal cause of the clinical failure of bioprosthetic heart valves fabricated from glutaraldehyde pretreated porcine aortic valves or bovine pericardium. The present study investigated controlled-release implants for prevention of the calcification of glutaraldehyde pretreated bovine pericardium in a rat subdermal model. Either Al3+ and Fe3+ (inhibitors of the growth and dissolution rate of hydroxyapatite crystals), levamisole (alkaline phosphatase inhibitor) or protamine sulphate (charge modifier) were individually incorporated into various polymeric carriers (either silicone rubber, polyurethane or silicone rubber-polyurethane copolymer). Polymeric implants were evaluated for in vitro release kinetics, which revealed that sustained drug release was obtained from 21 d to more than 90 d from various drug matrices. In vivo efficacy was studied by co-implanting the polymeric delivery systems with glutaraldehyde pretreated bovine pericardium for 21 d using a subdermal rat model; glutaraldehyde pretreated bovine pericardium calcium levels were quantitated by atomic absorption spectroscopy in the explanted tissues. Fe3+ and Al3+ polymeric implants were the most effective for inhibiting deposition of calcium mineral. Al3+ demonstrated 82% inhibition of calcification compared to controls and Fe3+ resulted in 80% inhibition of calcification. Specific histologic staining methods showed that Fe3+ and Al3+ were localized within the devitalized cells of the explanted glutaraldehyde pretreated bovine pericardium. No adverse effects on somatic growth or recipient bone morphology were noted following controlled-release drug administration. Controlled release of protamine sulphate or levamisole did not significantly inhibit glutaraldehyde pretreated bovine pericardium calcification. It is concluded that regional controlled release of Fe3+ or Al3+ inhibits glutaraldehyde pretreated bovine pericardium calcification in the rat subdermal model without adverse effects.

Aluminum

Modelling of the heart and pericardium at end-diastole.

Herein we present a refined version of Vito's two-sphere static model of the heart with pericardium and discuss its possible applications. The improvements we make on Vito's model are: (i) Vito assumed that the elastic materials which constitute the model 'heart' and 'pericardium' are isotropic; we relax this assumption to that of transverse-isotropy. (ii) Our analysis, which does not assume the existence of stored-energy functions, links the model directly to empirical stress-strain relations of suitable biaxial uniform-extension tests; two such stress-strain relations (one for the pericardium, one for the myocardium, both of which may be described by the same equation except for difference in the values of response parameters) now define the model completely, so we avoid altogether the difficult task of determining full-fledged constitutive equations for the pericardium and myocardium. As for applications, we contend that the concentric spheres in static equilibrium can be taken as a model of the left ventricle and pericardium at end-diastole. We show that the model when equipped with suitable stress-strain relations does give good fit to the pressure-volume data which Spotnitz et al. (1966, Circulation Res., 18, 49-66) obtained from excised canine left ventricles and to the pericardium data which Pegram et al. (1975, Circulation Res., 9, 707-714) obtained from closed chest, anaesthetized dogs. Three different empirical formulae were tried in the data-fitting as the equation that describes the requisite stress-strain relations. The 'exponential law' gave the best results.

Animals

Biaxial mechanical properties of human pericardium and canine comparisons.

The two-dimensional mechanical properties of human pericardium from seven males undergoing coronary artery bypass surgery were studied. A 25-mm square piece of parietal pericardium overlying the right ventricle was excised. An approximately 8-mm square target was marked at the center, and its dimension was measured electrooptically. When immersed in physiological saline at 37 degrees C, the specimen was subjected to biaxial isotropic loading. Large deformations developed in the beginning of the loading; the pericardium became increasingly stiffer when load was increased, and then became almost inextensible. As in canine pericardium [Lee et al., Am. J. Physiol. 249 (Heart Circ. Physiol. 18): H222-H230, 1985], hysteresis was present and tension-stretch relationship was insensitive to loading frequency during cyclic loading, relaxation of tension was substantial, and creep was insignificant. Unlike canine specimens, however, human pericardium was nearly isotropic and almost three times as thick [mean 0.55 +/- 0.02 mm (SD)]. The human tension-area relation for isotropic loading could be described by an exponential function and was found to shift significantly to the left of the canine. Therefore, human pericardium is less extensible than canine.

Adult

Restraining effect of intact pericardium during acute volume loading.

To determine the effect of the intact pericardium on ventricular end-diastolic pressures (EDP) during acute volume loading, we measured left ventricular (LV) and right ventricular (RV) micromanometer pressure and LV volume using a conductance catheter in eight open-chest, anesthetized dogs. A range of LV pressure and volume was obtained by intravascular volume expansion with the pericardium intact and then over a similar range after removal of the pericardium. Pericardial pressure (Pper) was calculated using static equilibrium analysis as the difference between LVEDP with the pericardium present and absent at a constant LV volume. At the beginning of the fluid infusion (LVEDP 7.3 +/- 1.7 mmHg and RVEDP 4.4 +/- 2.6 mmHg, mean +/- SD), Pper was not different from zero (-1.0 +/- 2.3 mmHg, P not significant). The onset of pericardial restraint (Pper greater than or equal to 0 mmHg) occurred when LVEDP was 9.1 +/- 2.9 mmHg and RVEDP was 4.1 +/- 2.9 mmHg. At low cardiac volumes before fluid infusion, RV transmural pressure was positive and significantly greater than the near zero Pper. After the onset of pericardial restraint, however, RVEDP and Pper increased similarly and were related according to Pper = 1.1 (+/- 0.34) RVEDP - 4.2 (+/- 2.6) mmHg, standard deviation 0.6 +/- 0.8 mmHg, r = 0.98 +/- 0.10. These data indicate that the intact pericardium behaves in two functionally distinct ways. At low cardiac volumes, Pper is zero and the pericardium does not affect LV filling. RV transmural pressure is positive and greater than Pper.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals

Effect of pericardium on regional myocardial systolic function in acute ischemia.

To know whether or not the pericardium affects regional myocardial systolic function in acute ischemia, we measured ischemic and non-ischemic segment lengths of the left ventricle using ultrasonic crystals in 10 open-chest dogs with the pericardium preserved. When the left ventricular pressure and segment lengths were stable after left circumflex coronary occlusion, we opened the pericardium widely. After coronary occlusion, end-diastolic length (EDL) in ischemic and non-ischemic segments increased, and the ischemic segment showed paradoxical systolic expansion while the non-ischemic segment increased its active shortening. After pericardiectomy, heart rate, left ventricular systolic pressure, and peak positive and negative dP/dt did not change. EDL in ischemic and non-ischemic segments further increased from 12.02 +/- 0.18 to 12.50 +/- 0.16 mm (mean +/- S.E., p less than 0.01) and from 11.12 +/- 0.20 to 11.45 +/- 0.18 mm (p less than 0.05), respectively, despite the concomitant fall in left ventricular end-diastolic pressure (LVEDP) from 12.4 +/- 0.6 to 10.6 +/- 0.8 mmHg (p less than 0.01). End-systolic length in ischemic and non-ischemic segments also increased from 12.37 +/- 0.25 to 12.70 +/- 0.20 mm (p less than 0.05) and from 8.50 +/- 0.13 to 8.74 +/- 0.13 mm (p less than 0.01), respectively, although the left ventricular end-systolic pressure did not change. Maximum expanded systolic length of the ischemic segment also increased from 12.99 +/- 0.20 to 13.42 +/- 0.16 mm (p less than 0.01). These results indicate that, in acute ischemia, the pericardium inhibits paradoxical systolic expansion of the ischemic region and increase in end-systolic length of non-ischemic segment. Thus, it is concluded that the pericardium modifies the regional myocardial systolic function in acute ischemia, perhaps through the mechanical restraint of the pericardium.

Animals

Jugular phlebogram in congenital absence of the pericardium.

The purpose of this study was to emphasize the diagnostic value of the jugular phlebogram in congenital absence of the pericardium. Phonocardiographic study was performed in seven patients with complete absence of the left pericardium and in four with partial pericardial defect (left sided in three, right sided in one). Associated heart lesions were absent in all patients. The characteristic features of the jugular phlebogram in these patients were decreased depth of x descent and tall v wave followed by deep y descent (M-shaped pattern). These jugular abnormalities were more prominent in complete absence of the left pericardium than in partial pericardial defect. The x descent was completely obliterated in two patients with complete left pericardial defect. Loss of decrease in pericardial pressure during ventricular ejection and altered cardiac position as a result of the absence of the pericardium may be responsible for these jugular abnormalities. Jugular venous M-shaped pattern may be one of the useful physical and phonocardiographic indicators for the diagnosis of congenital absence of the pericardium.

Adolescent

Reoperation after pericardial closure with bovine pericardium.

To reduce the risk of damage to the anterior surface of the right ventricle after resternotomy, it has been recommended that the pericardium be closed with a patch after open heart operations. We have examined 4 patients undergoing resternotomy for the third time 3 to 8 years after bovine pericardium valve replacement. On each occasion the pericardium was closed with a patch of bovine pericardium. In all cases, the patch was frozen to the inner aspect of the sternum, increasing the difficulty of resternotomy. Histological examinations of the patches confirmed dense fibrous connective tissue, patchy calcification, and foreign body giant cell reaction. Bovine pericardium appears to increase the difficulty of repeat cardiac operations. We recommend its use be discontinued.

Adult

Heterologous pericardium for the closure of pericardial defects.

Patches of glutaraldehyde-preserved porcine pericardium were transplanted orthotopically into 20 dogs to see if they might make a satisfactory pericardial substitute. Two dogs had mediastinal infections and were excluded from this study. All animals were reoperated on at regular intervals between 15 and 300 days. In 15 dogs there were no adhesions between the porcine pericardium and the host's epicardium. Histological study showed healing between both pericardiums and no degenerative changes in transplanted pericardium. Glutaraldehyde porcine pericardium has been utilized in 8 patients to close the pericardial cavity. There have been no problems related to the pericardial grafts after a maximum follow-up of 9 months.

Adult