Animal Evaluation of a New Pericardial Bioprosthe tic Heart Valve
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1 xh Page 1 Artificial Organs 12(4): , Raven Press, Ltd., New York nternational Society for Artificial Organs Animal valuation of a New Pericardial Bioprosthe tic Heart Valve T. J. Spyt, J. Fisher, "J. Reid, tj. D. Anderson, and D. J. Wheatley Department of Cardiac Surgery, Royal nfirmary, *Department of Veterinary Surgery, University of Glusgow, and?department of Pathology, Royal nfrmary,glasgow, U.K. Abstract: mplantation in animals is an essential step in the evaluation of any new prosthetic heart valve before commencing clinical trials. A new three-leaflet pericardial bioprosthesis developed in Glasgow has been implanted in the mitral position in ten sheep and eight dogs. leven animals were electively killed after 3 months of observation and explanted valves were in good condition. Hydro- dynamic tests of the explanted valves showed small changes in function compared to tests prior tc1 implantation. This was mainly due to host tissue ingrowth over the edge of the leaflets. Histological studies con&med good preservation of the pericardial tissue in explanted valves. Key Words: Pericardial bioprosthesis-animal evaluation. Since the first clinical use of artificial heart valves in 1960, there have been continuing developments in their design, reflecting their less than ideal function and propensity for complications. Before commencing clinical evaluation of a new design of valve, it is necessary to implant the valves in animals in order to look for any possible adverse features that could not be predicted from the laboratory, hydrodynamic, and fatigue tests that have been undertaken. Prosthetic heart valves have been implanted in both the left and right heart in sheep (l), dogs (2), calves (3), and goats (4). The best choice of animal model in which to evaluate a prosthetic heart valve, and the best site in the heart to test a new valve, remains controversial. Sheep have been widely used for studying calcification in bioprostheses. Calcification can occur within a few months in bioprosthetic valves when implanted in young, growing sheep (1,5-10). The incidence of calcification in bioprostheses implanted in mature sheep has not been reported. Although bioprostheses have been successfully implanted in dogs (2,9,11) it has been Received November 1987; revised March Address correspondence and reprint requests to Mr. T. J. Spyt, Senior Registrar, Department of Cardiac Surgery, Royal nfirmary, Glasgow G21 2R, U.K. suggested that they are prone to infection and thrombosis (9,12). Dogs usually require a smaller prosthetic heart valve than sheep. The heart in young calves of about 70 kg is similar in size to that of adult humans (3). However, the size of the calf can double during a 3 months implantation period, making the prosthesis relatively stenotic, and increasing the risk of paravalve leaks (13). Calcification can also occur very quickly in young calves (13,14). Valves have been implanted in both the mitral and tricuspid sites in all three animal models. The right ventricle does not produce the same pressures and stresses on the right atrioventricular valve as are obtained in the systemic: ventricle. Since high mechanical stresses can initlate tissue damage and calcification (15), the tricuspid site is not as demanding a test for the prosthesis as is the mitral site. A new pericardial bioprosthetic heart valve has been designed and developed in our Department and has been evaluated in vitro in our laboratory. The valve has a unique frame design with the valve leaflets mounted on an array of radically projecting pins, which allows leaflets to be interchanged during valve manufacture. Leaflets on each valve are matched for synchronous function under pulsable flow conditions during valve assembly. The frame is covered with a single piece of chemically treated 328 University of Michigan xhibit 2008 St. Jude Medical v. University of Michigan PR
2 xh Page 2 NW HART VALV 329 TABL 1. Haemodynamic measurements of cardiac output and maximum pressure difference across the valve prior to killing Maximum pressure difference during Cardiac output diastole Animal number (L/min) (mm Hg) Sheep Sheep Dog (thrombus) bovine pericardium. Laboratory tests have shown that the long-term durability of this new valve is superior to other pericardial valves, with the elimination of leaflet tears found in other valves, caused by abrasion of the leaflets at the edge of their clothcovered frames (16). Prior to clinical use of this new bioprosthetic valve, implantation was undertaken in ten sheep and eight dogs. Our experience and re- sults of this animal evaluation form the basis of this communication. MATRAL AND MTHODS Valve implantation in sheep The bioprosthesis was implanted in ten female Greyface sheep, aged months, and weighing kg. ach animal was deprived of food for 48 h, and water for 24 h, prior to operation. After premedication with diazepam, anaesthesia was induced with Methohexiton. A cuffed endotracheal tube was inserted with the animal supine and a stomach tube was placed in the dorsal sac of the rumen. Anaesthesia was maintained with 1-2% halothane in oxygen. The chest was entered through the fourth or fifth left intercostal space. xtracorporeal circulation was established with venous drainage through a cannula inserted via the pulmonary artery into the right ventricle and arte- FG. 1. Photograph of the outflow aspects of two explanted sheep valves (numbers 7 and 10). Valve 7 showed some calcification. Valve 10 was free from calcification. FG. 2. Radiograph ot two exptanreo sriaep vaivas (iiurrioers 7 and 10) showing some calcification in valve 7. ArtfOrgans, Vol. 12, No. 4, 1988
3 xh Page T. J. SPYT T AL. rial return into the descending aorta. A left ventricular vent was used to ensure decompression of the heart. A roller pump was used with a bubble oxygenator, cardiotomy reservoir, and arterial line fdter. The pump was primed with 2 L of Ringer s lactate solution with the addition of bicarbonate, mannitol, and heparin. During normothermic cardiopulmonary bypass, flow rates of L/min were achieved. Ventilation was discontinued and anaesthesia was maintained by halothane delivered through the gas inlet of the bubble oxygenator. The heart was electrically fibrillated to prevent air embolisation. The mitral valve was approached through an oblique incision from the tip of the appendage to its base. A 25 mm external diameter valve was inserted within the annulus, using interrupted mattress sutures buttressed with Teflon pledgets (2-0 Tycron, Davis & Geck, Hampshire, U.K.) placed on the ventricular surface. The prosthesis was orientated so that a scalloped interstrut portion spanned the left ventricular outflow tract. Postoperative pain was controlled by an intercostal nerve block before thoracotomy closure, and by the analgesics administered intramuscularly. The animals were given a 5 day course of antibiotics. No anticoagulant or antiplatelet drugs were given at any time in the postoperative period. At 3 months (17), the animals were anaesthetised and the chest was opened through the previous thoracotomy incision. Cardiac output was measured using the dye dilution technique. The pressure drop across the prosthesis was recorded by direct measurement of pressures in the left ventricle and the left atrium. The animal was then killed and a postmortem examination was carried out with particular attention to the appearance of the prosthesis and adjacent endocardium and evidence of systemic embolism. The hydrodynamic performance of each prosthesis used was measured in a pulsatile flow test apparatus (18) prior to implantation. These in vitro tests FG. 3. Photograph of the outflow aspect of two explanted dog valves (numbers 12 and 14) electively killed at 3 months. FG. 4. Radiograph of two explanted dog valves (numbers 12 and 14) both free from calcification. Artif Organs, Vol. 12, No. 4, 1988
4 xh Page 4 NW HART VALV 331 were repeated after implantation and the changes in forward flow pressure difference and regurgitant volumes were measured. Pulsatile flow tests were carried out at 60 beatslmin, a stroke volume of 60 ml, and a peak forward flow rate of 150 ml/s. This corresponds to a cardiac output of approximately 3 L/min. The mean pressure difference during forward flow and the regurgitant volumes per stroke were measured (18). Recordings of the valve leaflet dynamics were made on video tape. The valve was then preserved in 0.25% glutaraldehyde and a radiograph taken of the valve from the outflow surface to detect macroscopic calcification. The leaflets were then removed and a further radiograph was taken of individual leaflets. Valve leaflets were then examined histologically. Valve implantation in dogs The bioprosthesis was also implanted in the mitral site of eight dogs weighing kg. The procedure was similar to that described for the sheep. Twenty-one millimeter diameter valves were used. RSULTS Two sheep died shortly after surgery from respiratory failure. Their prosthetic valves were functioning normally. A third sheep developed prosthetic endocarditis and died 3 weeks after surgery. The remaining seven sheep were electively studied and killed at 13 or 14 weeks. Two dogs died shortly after surgery. n a third dog, the valve had been implanted with a suture inadvertently looped around one of the posts of the valve. This animal died 3 weeks after surgery with a thrombosed prosthesis and cerebral embolism. A fourth dog developed prosthetic endocarditis and died 3 months after surgery. ts prosthesis was obstructed by thrombus and vegetations. The remaining four dogs were electively studied and killed at 13 weeks. Table 1 gives the results of the haemodynamic tests on two sheep and one dog electively studied after 13 weeks. The appearance of the valves at the time of killing was generally good but in two of the dogs, thrombus wa_s visible adherent to the inflow aspect of the commissures. This thrombus significantly interfered with valve function in one dog, and this animal also showed multiple embolic infarcts in both kidneys. The valve thrombus grew Candida albicans on bacteriological culture. There was no thrombus adherent to any of the sheep implants. All of the valves implanted in both sheep and dogs showed smooth host tissue ingrowth over the sewing ring and extending 1-2 mm onto the ventricular surface of the base of the valve leaflets. Tissue TABL 2. Summary of hydrodynamic test results before implant and after explant Root mean square (RMS) Mean pressure Regurgitation Animal mplant/ flow difference Closing Closed number explant (mu,) (mm Hg) (ml) (ml) Sheep 2 Sheep 5 Sheep 6 Sheep 7 Sheep 8 Sheep 9 Sheep 10 Dog 12 Dog 13 Dog 14 Dog Not measured = prior to animal implantation, = following explantation o Artif Organs, Vol. 12, No. 4, 1988
5 332 T. J. SPYT T AL. ingrowth did not extend onto the pericardialcovered inflow aspect of the prostheses. Figure 1 shows the outflow aspect of two explanted sheep valves and Fig. 2 shows the radiographic appearance of the same two valves. A thin layer of host tissue covered the cloth sewing ring and outer sleeve-covering and extended up to 1 to 2 mm over the outflow surface of the leaflets at the edge of the frame. arly calcification was visible on the leaflets of four prostheses in sheep; none was seen on the dog implants. Calcification was seen at the commissures of valves 5, 6, and 7 and lower down the leaflets at the edge of the frame in valves 6 and 7. This was confirmed on the radiographic films, which also showed a small amount of calcification at the commissure of one leaflet in valve 8. Valves 9 and 10 FG. 5. Micrograph of pericardial tissue from an explanted sheep valve (a) and a control valve prior to implantation (b). The stain, x340. was haematoxylin and eosin; magnification was (a) ~ 2 7 0(b) Artf Organs, Vol. 12, No. 4, 1988 xh Page 5
6 xh Page 6 NW HART VALV lh extension ratio FG. 6. Result of uniaxial tensile tests on pericardial tissue before implantation and after explantation. The hatching shows the range of curves for tissue prior to implantation and after explantation. were free of macroscopic calcification. No calcification was found on pericardial coverings of the valve frame. Tissue ingrowth did not occur over the pericardial covering on the inflow aspect of the frame. Photographs of the outflow aspect of two valves implanted in dogs are shown in Fig. 3 and the radiographic appearances are shown in Fig. 4. Results of the hydrodynamic tests on the valves before implantation and after explantation are given in Table 2. The mean pressure difference across the valve was increased after explantation. n all valves, the difference was significant (p < 0.01, paired t test). n valves 2, 5, 6, and 7, this was caused by stiffening of the leaflets due to the calcification, while in the other sheep valves and dog valves, the tissue ingrowth over the edge of the leaflets restricted the full opening of the leaflets. The minimal pressure difference and flow required to open the valve leaflets was also greater in the explanted valves. Closing regurgitation was unchanged but the closed leakage was generally less as the tissue ingrowth sealed the cloth sewing ring. Histological studies showed that the collagen structure of the pericardial tissue was wellpreserved in the explanted valve leaflets (Fig. 5). The characteristic crimp of the collagen fibre bundles can be seen in both implanted and explanted FG. 7. Micrograph showing the presence of calcium in an explanted sheep valve leaflet. The stain was Von Kossa and rnagnification was ~ 300. Artf Organs, Vol. 12, No. 4, 1988
7 334 T. J. SPYT T AL. tissue. Mechanical tests showed that the tissue was significantly thickened and exhibited reduced extensibility after explantation. Tissue thickness was mm before implantation and 0.50 & 0.03 mm after explantation. The difference was signscant (p < 0.01, Student t test). The results of uniaxial tensile tests on 3 mm wide strips, cut circumferentially from the leaflets, are shown in Fig. 6 for control valves before implantation, antd sheep valves after explantation. There was a signifcant reduction in the mean extension ratio at 1.8 N force after explantation from compared to 22.9 & 4.95 in valves prior to implantation (p < 0.02, Student t test). This was probably due to permanent deformation of the relaxed length of the tissue after repeated cycling of the leaflets in vivo, and would * FG. 8. Scanning electron micrograph of the inflow surface of a control valve prior to implantation (a) and the outflow surface of an explanted sheep valve (b) (magnification ~2400). A r t f Organs, V o l. 12, No. 4, 1988 xh Page 7
8 xh Page 8 NW HART VALV 335 correspond to the loss of some of the crimp in the fibrils. Histological stains showed the presence of calcium in some of the explanted sheep valves (Fig. 7). Calcium was not found in the explanted dog valves. Scanning electron microscopy confirmed the histological findings of good preservation of the collagen structure in a control valve prior to implantation and in the explanted valves (Fig. 8). DSCUSSON mplantation in animals is an essential step in the evaluation of any new prosthetic valve prior to initial clinical evaluation (17). While detailed information about mechanical function and in vitro durability can be obtained in the laboratory, implantation in animals is the only way of studying the effect of biological processes such as calcification, thrombosis, and tissue ingrowth. No ideal animal model exists and our studies are in accord with the work of others showing that sheep show valve calcification at accelerated rates (1,5-10) while dogs have a risk of endocarditis and thrombosis (12). This new pericardial valve has shown similar hydrodynamic function but greatly improved durability in laboratory tests compared to other pericardial valves (16), and this study was carried out to test its short-term function in a biological environment prior to implantation in humans. The explanted sheep valves showed no thrombus. There were only small deposits of calcium and these had little effect on the hydrodynamic function of the explanted valves. The calcification appeared at various places on the valve leaflets although it tended to be close to the edge of the valve leaflet, where bending stresses were high. t has been suggested that high bending stresses cause calcification (15). No calcification was found on the pericardial covering of the valve frame, which is stationary and is not subject to cyclic loading or bending stresses. This is similar to the findings with polyurethane valves in calves, where the valve leaflets were heavily calcified, but stationary polyurethane material used to coat the valve frames did not calcify (19). While the explanted dog valves were free from Calcification, one valve was thrombosed with associated infection, and small amounts of thrombus were found at the commissures of a second valve. This did not affect leaflet function in the hydrodynamic tests. Hydrodynamic tests of the explanted valves showed changes in function compared to the same valves tested prior to implantation. Host tissue ingrowth on the outflow surface of the leaflet at the edge of the frame restricted the portion of the leaflet that could flex to the open position. This caused a significant increase in the measured pressure difference after explantation. The thickening and reduction in extensibility of the explanted leaflets probably contributed to the increased pressure difference and increased minimal flow required to open the leaflets. The reduction in extensibility of the explanted tissue is probably due to a permanent deformation of the unloaded leaflet and loss of some of the crimp in the collagen structure. The host tissue ingrowth sealed the sewing ring and reduced the closed valve regurgitation in the explanted valves. Histological examination showed good preservation of the collagen structure. The animal implant studies have shown satisfactory short-term performance of this pericardial valve. This pericardial valve is now being used in clinical practice. RFRNCS 1. Jones M, Barnhart GR, Chaves AM, et al. xperimental evaluation of bioprosthetic valves in sheep. n: Cohn LH, Galluci V, eds. Cardiac bioprosfheses. New York: Yorke Medical Books, 1982; Okamura K, Yuge, Kawazoe H, Kitamura N, mamura, Konno S. A comparative study between glutaraldehyde preserved aortic and pulmonary heterograft valves in dogs. J Cardiovasc Surg 1976;17: Yarborough JN, Roberts WC, Reis RL. Structural alterations in tissue cardiac valves implanted in patients and in calves. J Thorac Cardiovasc Surg 1973;65: Macver AG, Howarth WS. The fate of prosthetic leaflet heart valves implanted in animals. n: Williams D, ed. Biocompatibility of implant materials. London: Sector Publishing, 1985: Barnhart GR, shihara T, Ferrans VJ, Jones M, Mcntosh CL, Roberts WC. ntracuspal hematomas in bioprosthetic valves. Pathological findings and clinical implications. Circulation 1982;66(suppl 1): Barnhart GR, Jones M, shihara T, Rose DM, Chavez AM, Ferrans VJ. Degeneration and calcification of bioprosthetic cardiac valves. Am J Pathot 1982;106: Barnhart GR, Jones M, shihara T, Chavez AM, Rose DM, Ferrans VJ. Failure of porcine aortic and bovine pericardial valves. An experimental model in young sheep. Circulation 1982;66(suppl 1): Barnhart GR, Jones M, lshihara T, Chavez AM, Rose DM, Ferrans VJ. Bioprosthetic valve failure. J Thorac Cardiovasc Surg 1982;83: Gabbay S, Bortolotti U, Cipolletti G, Wasserman F, Frater RWM. The Meadox unicusp pericardial bioprosthetic heart valve. Ann Thoruc Slug 1984;37: Jones M, idbo, Walters SM, Ferrans VJ, Clark R. ffects of two types of pre-implantation processes on calcification of bioprosthetic valves. n: Yacoub M, Bodnar, eds. Biological and bioprosthefic valves. New York: Yorke Medical Books, 1986: Reece J, Anderson JD, Wain WH, et al. A new porcine bioprosthesis: in vitro and in vivo evaluation. Life Support Syst 1985;3: Artf Organs, Vol. 12, No. 4, 1988
9 xh Page T. J. SPYT T AL. 12. Hancock JB, Forshaw PL, Kay MP. Gore-Tex in canine coronary artery bypass. J Thorac Cardiovasc Surg 1980;80: Boncheck L, Tatooles CJ, Braunwuld NS. xperimental cardiac surgery in the calf. Ann Thorac Surg 1967;3: Black M, Drury PJ, Lawford PV, Wain WH. The design, development and animal testing of the Shefield-Wessex Bioprosthesis. Life Support Syst 1986;4: Deck JD, Thubrikar MJ, Nolan SP, Aouad J. Role of mechanical stress in calcification of bioprostheses. n: Cohn LN, Galluci V, eds. Cardiac bioprosrheses. New York: Yorke Medical Books, 1982: Fisher J, Wheatley DJ. An improved pencardial bioprosthetic heart valve, design and laboratory evaluation. ur J Cardiovasc Surg 1987;1: Draft nternational Standard S0 5840, Cardiac Valve Prostheses, October Fisher J, Reece J, Wheatley DJ. n vitro evaluation of six mechanical and six bioprosthetic valves. Thoruc Cardiovasc Surg 1986;34: Herold M, Lo HB, Reul H, et al. The Helmholtz nstitute tri-leaflet polyurethane heart valve prosthesis. Proceedings of the 1 nternational Conference Polyurethanes in Biomedical ngineering, Stuttgart, West Germany, Artif Organs, Vo. 12, NO. 4, 1988
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