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Cuspal perforations caused by long suture ends in implanted bioprosthetic valves
J
THoRAc CARDIOVASC SURG
90:557-563, 1985
Cuspal perforations caused by long suture ends in implanted bioprosthetic valves A description is presented of thegross anatomic, histologic, and scanning electron microscopic features of abrasions, perforations, and tears caused by excessively long ends of braided sutures in bioprosthetic cardiac valves implanted in the mitral position in sheep. These lesions are produced as comequences of contact between theends of thesutures and theinflow surfaces of thebioprosthetic cusps, leading to a process of surface erosion thatprogresses to actual perforation of the cusps. The perforation has theappearance of a crater, thewider end of which faces the inflow surface and thewalls of which are formed by broken ends of coUagen fibrils. Suture perforations can extend to form tears that involve the free edge of the cusp and result in hemodynamicaUy important regurgitation. Therefore, care must be taken to avoid leaving excessively long suture ends during the implantation of bioprosthetic cardiac valves. Clfipal
Michael Jones, M.D., E. Rene Rodriguez, M.D., Elling E. Eidbo, BA, and Victor J. Ferrans, M.D., Ph.D., Bethesda, Md.
Eforations of the cusps of cardiac valvular bioprostheses by excessively long ends of sutures have been reported as rare complications of aortic valvular replacement.!-? This communication describes the gross anatomic, histologic, and scanning electron microscopic appearance of cuspal perforations caused by long ends by braided Tevdek sutures (Deknatel Division of Howmedica, Floral Park, N. Y.) in bioprosthetic valves implanted in the mitral position and discusses the surgical implications of this complication.
Materials and methods Among approximately 450 bioprostheses that have been explanted from sheep undergoing atrioventricular valvular replacement as part of our evaluation of different types of bioprostheses;" we have encountered two bioprostheses that had been implanted in the mitral position and that had cuspallesions related to excessively long suture ends (Valves 1 and 2). An additional valve (No.3) developed similar lesions after excessively long suture ends were intentionally allowed to remain at the From the Surgery and Pathology Branches, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md. Received for publication Oct. 8, 1984. Accepted for publication Jan. 21, 1985. Address for reprints: Michael Jones, M.D., Building 10, Room 2N242, National Institutes of Health, Bethesda, Md., 20205.
time of implantation to establish the pathogenesis of these lesions in vivo. The techniques utilized for the bioprosthetic implantation and for analyses of the explanted bioprostheses have been described in detail elsewhere.'? At the time of autopsy, each bioprosthesis was removed, photographed, fixed with glutaraldehyde, and examined grossly and with a dissecting microscope (up to X40). For scanning electron microscopic study, the cusps were detached, dried according to the critical-point method, coated on both surfaces with gold-palladium, and mounted on aluminum studs. After both surfaces were examined by scanning electron microscopy, each cusp was placed in absolute ethanol, sectioned carefully with a razor blade along the plane of the perforation, and embedded in glycol methacrylate. Histologic sections were stained with hematoxylin and eosin or with alkaline toluidine blue.
Results Valve 1, a porcine aortic valvular bioprosthesis (Hancock/Extracorporeal, 25 rom), had been implanted for 20 weeks. At the time of terminal elective study, moderate mitral regurgitation (radiographic material filling the left atrium but not the pulmonary veins) was found by ventriculography. The mean diastolic pressure gradient across the valve was 6.5 rom Hg and the valve area calculated by the Gorlin and Gorlin formula in the presence of the regurgitation was 0.94 em'. Roentgeno557
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Fig. 1. Valve 1. A, Inflow surface, showing perforation associated with the free end of a suture. B, Suture-induced perforation as seen with dissecting microscope. The braided multifilament suture is partially covered by a white fibrous sheath. A tear is present at the free edge of the left coronary cusp (upper right). A perforation in the right coronary cusp is adjacent to the end of the suture. (Original magnification XI5.)
Fig. 2. Histologic section through the area of perforation in the right coronary cusp of Valve I. The inflow surface is at the bottom and the outflow surface at the top. A fibrous sheath extends on both surfaces of the basal region of the cusps (left). The erosion has caused loss of the ventricularis layer (arrowheads) on the inflow surface and a perforation that extends through all layers of the cusp. (Hematoxylin and eosin stain; original magnification XS.)
grams of the excised valve showed multiple areas of calcification localized in the base and tip of the right coronary cusp and in all three commissures. The bioprosthetic cusps showed mild retraction. Quantitative calcium analyses revealed 93 mg of calcium per gram of tissue dry weight (mean value obtained from analyses of one half of each cusp). There were two perforations in the right coronary cusp and a tear at the free edge of the left coronary cusp (Fig. 1). Histologic study (Fig. 2) showed that both surfaces of the basal regions of the cusps were covered by a fibrous sheath, which was partially lined by endothelium. The endothelial layer ended abruptly in the vicinity of the perforation, where a few, small fibrin deposits were
present together with scanty erythrocytes and leukocytes. Occasionally macrophages and erythrocytes were also found within the substance of the cusp. Calcific deposits were not present in the vicinity of the perforation. Scanning electron microscopic study (Fig. 3) of the right coronary cusp showed two closely adjacent perforations and absence of endothelium from a large portion of the inflow surface. The smaller perforation measured 600 JLm in its largest dimension. The second perforation measured 2,000 JLm by 800 JLm. On the inflow surface, the two perforations were surrounded by an area of exposed, partially eroded collagen that measured 7 mm in diameter. The zones of erosion involving the tissue layers of the cusp formed two broad craters at the sites
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Fig. 3. Scanning electron micrographs of the inflow (A, C, E) and outflow (B, D, F) surfaces of the perforation in Valve 1. A and B are matching views of the same area of the cusp, comparing the eroded aspect of the inflow surface (A) and the smooth appearance of the outflow surface (B). C and D also are matching views of the same area (nearest the center of the page in A and B). A developing tear is seen on the inflow surface (C) but is much more evident on the outflow surface (D). E, Higher magnification view of the area near the center of C, showing that the inflow surface is formed by disrupted, fragmented bundles of collagen. F, Endothelial lining layer in area of the outflow surface. (Original magnifications: A and B, x20; C and D, X60; E and F, X300.)
of perforation. The walls of these craters sloped gradually and were composed of collagen bundles with broken, fragmented ends. The exposed collagen was associated with small deposits of fibrin but with only very few platelets. An elongated tear appeared to be in the process of developing at one of the ends of the larger perforation. Beyond the edges of the eroded area and toward the base of the cusp, a uniform layer of endothelial cells covered the inflow surface of the cusp. The endothelial layer on the outflow surface of the cusp
extended to the periphery of the perforations, ending abruptly at about 100 Jlm of their edges. Valve 2 was a Carpentier-Edwards bovine pericardial bioprosthesis (25 mm), which had been implanted for 16 weeks. The animal died of cardiopulmonary failure, resulting from calcific bioprosthetic stenosis, before hemodynamic studies could be performed. Roentgenographic examination showed severe calcification throughout each cusp. Mean calcium content (analysis of one half of each cusp) was 68 mg per gram of tissue
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The Journal of Thoracic and Cardiovascular Surgery
Fig. 4. Valve 2. A, Inflow surface showing a long suture end in contact with the cusp (top center). B, Dissecting microscopic view of small areas of surface abrasion immediately to the right of the end of the suture. (Original magnification X20.)
Fig. 5. Valve 3. A, Inflow surface, showing calcific deposits (raised white areas) in the cusps, a small perforation (to the right of center) and several suture ends which were intentionally left excessively long at the time of implantation. B, Dissecting microscopic view of cuspal lesion in A, showing that it consists of at least two perforations surrounded by an area of abrasion. The bioprosthesis has been tilted to an angle to best demonstrate the perforations (compare with Fig. 7, which shows scanning electron micrographs of the same perforations). (Original magnification xlO.)
dry weight. No perforation was present, but an abrasion caused by a long suture end was observed on the inflow surface of a cusp during examination with a dissecting microscope (Fig. 4). Valve 3, a Xenotech, toluidine blue-treated, porcine aortic valvular bioprosthesis (25 mm), had been implanted for 16 weeks. Several excessively long suture ends had been left intentionally at the time of implanta-
tion. At the time of terminal elective study, trivial bioprosthetic regurgitation was noted by left ventriculography. The mean diastolic pressure gradient across the valve was 9 mm Hg and the calculated valve orifice area (Godin and Godin formula) was 0.92 cm-. Roentgenographic examination showed severe calcification in the left and right coronary cusps and moderate calcification in the noncoronary cusp, with extensive involvement of
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Cuspal perforations 5 6 1
October, 1985
Fig. 6. Histologic section through region of perforation in cusp of Valve 3. The inflow surface of the cusp is shown at the bottom, the outflow surface at the top. The nodular masses to the right and left of the perforaton are calcific deposits, which have extended from the spongiosa to adjacent layers of the cusp. The perforation is at the center of an area of marked erosion of the inflow surface (Hematoxylin and eosin stain; original magnification xlO.)
Fig. 7. Scanning electron micrographs of the inflow (A and C) and outflow (B and D) surfaces in the region of cuspal perforation in Valve 3. A. Perforation appears as a deep crater with severely eroded walls. Two smaller perforations are also seen. B. Same perforation as in A but viewed from the outflow surface, which has a smoother appearance. C, Higher magnification view of right border of perforation shown in A. This area of the inflow surface is highly irregular and devoid of endothelium. D, Part of the lower border of the perforation illustrated in B. The surface is less severely eroded than that shown in C. (Original magnifications: A and B. x45; C, X200; D, x300.)
all commissures. Two small perforations, related to a long suture end on the inflow surface, were present, one in the right coronary cusp, the other in the left coronary cusp (Fig. 5). Histologic study (Fig. 6) showed several large, calcific nodules, which were localized mainly in
the spongiosa but also extended into the ventricularis and the fibrosa. These nodules projected above both surfaces, particularly the outflow surface. One of these nodules was located close to the edge of a perforation. A fibrous sheath was not present. The areas of perforation
The Journal of Thoracic and Cardiovascular Surgery
5 6 2 Jones et al.
consisted of broad craters with progressive loss of tissue toward their central regions. Scanning electron microscopic examination (Fig. 7) confirmed that the perforations consisted of broad craters with erosion of collagenous tissue toward their central regions. The calcific deposits had highly irregular surfaces. Both surfaces of the cusps were focally and irregularly lined by endothelium. The perforations were partially surrounded by calcific material and were morphologically similar to those found in Valve 1.
Discussion Cuspal perforations that had been caused by excessively long suture ends in bioprosthetic cardiac valves implanted in the aortic position were first described in a bulletin issued by American Edwards Laboratories I and were subsequently reported by ROSS.2 These perforations were found in bioprostheses that had been submitted to American Edwards Laboratories for examination. The perforations were reproduced in a pulse duplicator with valves in which monofilament polypropylene (Prolene, Ethicon, Inc., Somerville, N. J.) sutures had been placed. It was suggested that such perforations were less likely to occur if multifilament braided sutures were used, because such sutures are less rigid and might be less traumatic, at least initially." However, multifilament sutures become more rigid as they become encapsulated by the ingrowth of fibrous tissue that develops on the sewing ring after implantation. One of the perforations reported by American Edwards Laboratories was caused by a multifilament suture. I Multifilament braided sutures were used to implant the bioprostheses in the three sheep in the present study. Our study also shows that suture perforations can develop in bioprostheses implanted in the mitral position, in which the free ends of the sutures are on the inflow surfaces of the bioprostheses. This is in contrast to bioprostheses implanted in the aortic position, in which the free ends of the sutures are on the outflow surface. The sewing rings of valves designed for the aortic position may be smaller than those of valves designed for the mitral position. Therefore, the length of the free ends of the sutures probably is more critical in the aortic position, because the length of the suture ends that can cause perforations may be shorter in aortic bioprostheses than in mitral bioprostheses. Contact between the suture end and the cusp may be increased if the cusp becomes rigid and immobile because of calcification. This appeared to have occurred in Valve 3 in the present study, in which the sutures intentionally had been left long. However, perforations also can occur in areas where the cuspal connective tissue is normal, as was the
case in Valve I. The appearance of the cuspal surfaces in regions of suture damage is consistent with the concept that repeated contact between the suture end and the cuspal tissue leads to gradual abrasion and erosion of the surface. The resulting loss of tissue can produce not only perforation, but also further damage, perhaps related to repeated mechanical bending of the weakened area of the cusp (as shown by the developing tear found in Valve 1). The areas of erosion on the inflow surfaces were much larger than the areas of actual perforation. This appears to reflect the patterns of relative motion of the cusps and the suture ends with respect to each other during the systolic and diastolic phases of the cardiac cycle. The fmdings in Valve I indicate that hemodynamically important valvular regurgitation can result from suture perforations. This observation is in accord with previous experience with this problem, which resulted in a second aortic valvular replacement in at least two
patients.': 2 The morphology of the areas of the inflow surface that were in contact with the elongated suture ends differed from that seen in other types of perforations and tears that have been described in bioprostheses implanted in patients.'? Perforations associated with infection are much more irregular and contain abundant fibrin and inflammatory cells. Tears and perforations related to mechanical stresses in localized regions of the cusps also have fragmented ends of collagen on their surfaces (and also may be associated with calcific deposits). However, in our experience the latter lesions lack the crater-like appearance, with the broader end on the inflow surface, and the relatively even distribution of the collagen erosion that we observed in suture-induced perforations in bioprostheses implanted in the mitral position. The conclusions of this study are summarized as follows: (I) Cuspal perforations can be induced by excessively long suture ends in bioprostheses implanted in the mitral as well as in the aortic position; (2) such damage can occur both in pericardial and in porcine aortic valvular bioprostheses; (3) the lesions are morphologically characterized by a crater-like appearance, with the broader end of the crater adjacent to the elongated suture end; (4) the resulting lesions can be hemodynamically significant; and (5) care must be taken not to leave excessively long suture ends during implantation of bioprosthetic valves.
Addendum A recent bulletin from American Edwards Laboratories (Carpentier-Edwards Bioprostheses Clinical Report, January, 1985, 272-10/84-CV) has reported a total of 80 suture-related
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abrasions. Seventy-seven of these valves had been implanted in the aortic position and the other three in the mitral position. Therefore, these abrasions are more common than was previously thought to be the case. 6 REFERENCES
2
3
4
5
American Edwards Laboratories Technical Bulletin 106159-1, August, 1979 Ross DN: Panel discussion, Bioprosthetic Cardiac Valves, F Sebening, WP Klovekorn, H Meisner, E Struck, eds., Munich, 1979, Deutsches Herzzentrum, p 382 Barnhart GR, Jones M, Ishihara T, Rose DM, Chaves AM, Ferrans VJ: Animal model of human disease. Degeneration and calcification of bioprosthetic cardiac valves. Bioprosthetic tricuspid valve implantation in sheep. Am J Pathol 106:136-139, 1982 Barnhart GR, Jones M, Ishihara T, Chavez AM, Rose DM, Ferrans VJ: Bioprosthetic valvular failure. Clinical and pathological observations in an experimental animal model. J THORAC CARDIOVASC SURG 83:602-609, 1982 Jones M, Barnhart GR, Chavez AM, Jett JK, Rose DM, Ishihara T, Ferrans VJ: Experimental evaluation of bio-
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8
9
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prosthetic valves implanted in sheep. Cardiac Bioprostheses, Proceedings of the Second International Symposium, LH Cohn, V Gallucci, eds., New York, 1982, Yorke Medical Books, pp 331-345 Arbustini E, Jones M, Eidbo EE, Carroll RJ, Ferrans VJ: Modification by the Hancock T6 process of calcification of bioprosthetic cardiac valves implanted in sheep. Am J Cardiol 53:1388-1396, 1984 Arbustini E, Jones M, Ferrans VJ: Formation of cartilage in bioprosthetic cardiac valves implanted in sheep. A morphologic study. Am J Cardiol 52:632-636, 1983 Ferrans VJ, Spray TL, Billingham ME, Roberts WC: Structural changes in glutaraldehyde-treated porcine heterografts used as substitute cardiac valves. Transmission and scanning electron microscopic observations in 12 patients. Am J Cardiol 41:1159-1184, 1978 Carpentier A: Panel discussion, Bioprosthetic Cardiac Valves, F Sebening, WP Klovekorn, H Meisner, E Struck, eds., Munich, 1979, Deutsches Herzzentrum, p 382 Ishihara T, Ferrans VJ, Boyce SW, Jones M, Roberts WC: Structure and classification of cuspal tears and perforations in porcine bioprosthetic cardiac valves implanted in patients. Am J Cardiol 48:665-678, 1981
THoRAc CARDIOVASC SURG
90:557-563, 1985
Cuspal perforations caused by long suture ends in implanted bioprosthetic valves A description is presented of thegross anatomic, histologic, and scanning electron microscopic features of abrasions, perforations, and tears caused by excessively long ends of braided sutures in bioprosthetic cardiac valves implanted in the mitral position in sheep. These lesions are produced as comequences of contact between theends of thesutures and theinflow surfaces of thebioprosthetic cusps, leading to a process of surface erosion thatprogresses to actual perforation of the cusps. The perforation has theappearance of a crater, thewider end of which faces the inflow surface and thewalls of which are formed by broken ends of coUagen fibrils. Suture perforations can extend to form tears that involve the free edge of the cusp and result in hemodynamicaUy important regurgitation. Therefore, care must be taken to avoid leaving excessively long suture ends during the implantation of bioprosthetic cardiac valves. Clfipal
Michael Jones, M.D., E. Rene Rodriguez, M.D., Elling E. Eidbo, BA, and Victor J. Ferrans, M.D., Ph.D., Bethesda, Md.
Eforations of the cusps of cardiac valvular bioprostheses by excessively long ends of sutures have been reported as rare complications of aortic valvular replacement.!-? This communication describes the gross anatomic, histologic, and scanning electron microscopic appearance of cuspal perforations caused by long ends by braided Tevdek sutures (Deknatel Division of Howmedica, Floral Park, N. Y.) in bioprosthetic valves implanted in the mitral position and discusses the surgical implications of this complication.
Materials and methods Among approximately 450 bioprostheses that have been explanted from sheep undergoing atrioventricular valvular replacement as part of our evaluation of different types of bioprostheses;" we have encountered two bioprostheses that had been implanted in the mitral position and that had cuspallesions related to excessively long suture ends (Valves 1 and 2). An additional valve (No.3) developed similar lesions after excessively long suture ends were intentionally allowed to remain at the From the Surgery and Pathology Branches, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md. Received for publication Oct. 8, 1984. Accepted for publication Jan. 21, 1985. Address for reprints: Michael Jones, M.D., Building 10, Room 2N242, National Institutes of Health, Bethesda, Md., 20205.
time of implantation to establish the pathogenesis of these lesions in vivo. The techniques utilized for the bioprosthetic implantation and for analyses of the explanted bioprostheses have been described in detail elsewhere.'? At the time of autopsy, each bioprosthesis was removed, photographed, fixed with glutaraldehyde, and examined grossly and with a dissecting microscope (up to X40). For scanning electron microscopic study, the cusps were detached, dried according to the critical-point method, coated on both surfaces with gold-palladium, and mounted on aluminum studs. After both surfaces were examined by scanning electron microscopy, each cusp was placed in absolute ethanol, sectioned carefully with a razor blade along the plane of the perforation, and embedded in glycol methacrylate. Histologic sections were stained with hematoxylin and eosin or with alkaline toluidine blue.
Results Valve 1, a porcine aortic valvular bioprosthesis (Hancock/Extracorporeal, 25 rom), had been implanted for 20 weeks. At the time of terminal elective study, moderate mitral regurgitation (radiographic material filling the left atrium but not the pulmonary veins) was found by ventriculography. The mean diastolic pressure gradient across the valve was 6.5 rom Hg and the valve area calculated by the Gorlin and Gorlin formula in the presence of the regurgitation was 0.94 em'. Roentgeno557
558 Jones et al.
The Journal of Thoracic and Cardiovascular Surgery
Fig. 1. Valve 1. A, Inflow surface, showing perforation associated with the free end of a suture. B, Suture-induced perforation as seen with dissecting microscope. The braided multifilament suture is partially covered by a white fibrous sheath. A tear is present at the free edge of the left coronary cusp (upper right). A perforation in the right coronary cusp is adjacent to the end of the suture. (Original magnification XI5.)
Fig. 2. Histologic section through the area of perforation in the right coronary cusp of Valve I. The inflow surface is at the bottom and the outflow surface at the top. A fibrous sheath extends on both surfaces of the basal region of the cusps (left). The erosion has caused loss of the ventricularis layer (arrowheads) on the inflow surface and a perforation that extends through all layers of the cusp. (Hematoxylin and eosin stain; original magnification XS.)
grams of the excised valve showed multiple areas of calcification localized in the base and tip of the right coronary cusp and in all three commissures. The bioprosthetic cusps showed mild retraction. Quantitative calcium analyses revealed 93 mg of calcium per gram of tissue dry weight (mean value obtained from analyses of one half of each cusp). There were two perforations in the right coronary cusp and a tear at the free edge of the left coronary cusp (Fig. 1). Histologic study (Fig. 2) showed that both surfaces of the basal regions of the cusps were covered by a fibrous sheath, which was partially lined by endothelium. The endothelial layer ended abruptly in the vicinity of the perforation, where a few, small fibrin deposits were
present together with scanty erythrocytes and leukocytes. Occasionally macrophages and erythrocytes were also found within the substance of the cusp. Calcific deposits were not present in the vicinity of the perforation. Scanning electron microscopic study (Fig. 3) of the right coronary cusp showed two closely adjacent perforations and absence of endothelium from a large portion of the inflow surface. The smaller perforation measured 600 JLm in its largest dimension. The second perforation measured 2,000 JLm by 800 JLm. On the inflow surface, the two perforations were surrounded by an area of exposed, partially eroded collagen that measured 7 mm in diameter. The zones of erosion involving the tissue layers of the cusp formed two broad craters at the sites
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Fig. 3. Scanning electron micrographs of the inflow (A, C, E) and outflow (B, D, F) surfaces of the perforation in Valve 1. A and B are matching views of the same area of the cusp, comparing the eroded aspect of the inflow surface (A) and the smooth appearance of the outflow surface (B). C and D also are matching views of the same area (nearest the center of the page in A and B). A developing tear is seen on the inflow surface (C) but is much more evident on the outflow surface (D). E, Higher magnification view of the area near the center of C, showing that the inflow surface is formed by disrupted, fragmented bundles of collagen. F, Endothelial lining layer in area of the outflow surface. (Original magnifications: A and B, x20; C and D, X60; E and F, X300.)
of perforation. The walls of these craters sloped gradually and were composed of collagen bundles with broken, fragmented ends. The exposed collagen was associated with small deposits of fibrin but with only very few platelets. An elongated tear appeared to be in the process of developing at one of the ends of the larger perforation. Beyond the edges of the eroded area and toward the base of the cusp, a uniform layer of endothelial cells covered the inflow surface of the cusp. The endothelial layer on the outflow surface of the cusp
extended to the periphery of the perforations, ending abruptly at about 100 Jlm of their edges. Valve 2 was a Carpentier-Edwards bovine pericardial bioprosthesis (25 mm), which had been implanted for 16 weeks. The animal died of cardiopulmonary failure, resulting from calcific bioprosthetic stenosis, before hemodynamic studies could be performed. Roentgenographic examination showed severe calcification throughout each cusp. Mean calcium content (analysis of one half of each cusp) was 68 mg per gram of tissue
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The Journal of Thoracic and Cardiovascular Surgery
Fig. 4. Valve 2. A, Inflow surface showing a long suture end in contact with the cusp (top center). B, Dissecting microscopic view of small areas of surface abrasion immediately to the right of the end of the suture. (Original magnification X20.)
Fig. 5. Valve 3. A, Inflow surface, showing calcific deposits (raised white areas) in the cusps, a small perforation (to the right of center) and several suture ends which were intentionally left excessively long at the time of implantation. B, Dissecting microscopic view of cuspal lesion in A, showing that it consists of at least two perforations surrounded by an area of abrasion. The bioprosthesis has been tilted to an angle to best demonstrate the perforations (compare with Fig. 7, which shows scanning electron micrographs of the same perforations). (Original magnification xlO.)
dry weight. No perforation was present, but an abrasion caused by a long suture end was observed on the inflow surface of a cusp during examination with a dissecting microscope (Fig. 4). Valve 3, a Xenotech, toluidine blue-treated, porcine aortic valvular bioprosthesis (25 mm), had been implanted for 16 weeks. Several excessively long suture ends had been left intentionally at the time of implanta-
tion. At the time of terminal elective study, trivial bioprosthetic regurgitation was noted by left ventriculography. The mean diastolic pressure gradient across the valve was 9 mm Hg and the calculated valve orifice area (Godin and Godin formula) was 0.92 cm-. Roentgenographic examination showed severe calcification in the left and right coronary cusps and moderate calcification in the noncoronary cusp, with extensive involvement of
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Fig. 6. Histologic section through region of perforation in cusp of Valve 3. The inflow surface of the cusp is shown at the bottom, the outflow surface at the top. The nodular masses to the right and left of the perforaton are calcific deposits, which have extended from the spongiosa to adjacent layers of the cusp. The perforation is at the center of an area of marked erosion of the inflow surface (Hematoxylin and eosin stain; original magnification xlO.)
Fig. 7. Scanning electron micrographs of the inflow (A and C) and outflow (B and D) surfaces in the region of cuspal perforation in Valve 3. A. Perforation appears as a deep crater with severely eroded walls. Two smaller perforations are also seen. B. Same perforation as in A but viewed from the outflow surface, which has a smoother appearance. C, Higher magnification view of right border of perforation shown in A. This area of the inflow surface is highly irregular and devoid of endothelium. D, Part of the lower border of the perforation illustrated in B. The surface is less severely eroded than that shown in C. (Original magnifications: A and B. x45; C, X200; D, x300.)
all commissures. Two small perforations, related to a long suture end on the inflow surface, were present, one in the right coronary cusp, the other in the left coronary cusp (Fig. 5). Histologic study (Fig. 6) showed several large, calcific nodules, which were localized mainly in
the spongiosa but also extended into the ventricularis and the fibrosa. These nodules projected above both surfaces, particularly the outflow surface. One of these nodules was located close to the edge of a perforation. A fibrous sheath was not present. The areas of perforation
The Journal of Thoracic and Cardiovascular Surgery
5 6 2 Jones et al.
consisted of broad craters with progressive loss of tissue toward their central regions. Scanning electron microscopic examination (Fig. 7) confirmed that the perforations consisted of broad craters with erosion of collagenous tissue toward their central regions. The calcific deposits had highly irregular surfaces. Both surfaces of the cusps were focally and irregularly lined by endothelium. The perforations were partially surrounded by calcific material and were morphologically similar to those found in Valve 1.
Discussion Cuspal perforations that had been caused by excessively long suture ends in bioprosthetic cardiac valves implanted in the aortic position were first described in a bulletin issued by American Edwards Laboratories I and were subsequently reported by ROSS.2 These perforations were found in bioprostheses that had been submitted to American Edwards Laboratories for examination. The perforations were reproduced in a pulse duplicator with valves in which monofilament polypropylene (Prolene, Ethicon, Inc., Somerville, N. J.) sutures had been placed. It was suggested that such perforations were less likely to occur if multifilament braided sutures were used, because such sutures are less rigid and might be less traumatic, at least initially." However, multifilament sutures become more rigid as they become encapsulated by the ingrowth of fibrous tissue that develops on the sewing ring after implantation. One of the perforations reported by American Edwards Laboratories was caused by a multifilament suture. I Multifilament braided sutures were used to implant the bioprostheses in the three sheep in the present study. Our study also shows that suture perforations can develop in bioprostheses implanted in the mitral position, in which the free ends of the sutures are on the inflow surfaces of the bioprostheses. This is in contrast to bioprostheses implanted in the aortic position, in which the free ends of the sutures are on the outflow surface. The sewing rings of valves designed for the aortic position may be smaller than those of valves designed for the mitral position. Therefore, the length of the free ends of the sutures probably is more critical in the aortic position, because the length of the suture ends that can cause perforations may be shorter in aortic bioprostheses than in mitral bioprostheses. Contact between the suture end and the cusp may be increased if the cusp becomes rigid and immobile because of calcification. This appeared to have occurred in Valve 3 in the present study, in which the sutures intentionally had been left long. However, perforations also can occur in areas where the cuspal connective tissue is normal, as was the
case in Valve I. The appearance of the cuspal surfaces in regions of suture damage is consistent with the concept that repeated contact between the suture end and the cuspal tissue leads to gradual abrasion and erosion of the surface. The resulting loss of tissue can produce not only perforation, but also further damage, perhaps related to repeated mechanical bending of the weakened area of the cusp (as shown by the developing tear found in Valve 1). The areas of erosion on the inflow surfaces were much larger than the areas of actual perforation. This appears to reflect the patterns of relative motion of the cusps and the suture ends with respect to each other during the systolic and diastolic phases of the cardiac cycle. The fmdings in Valve I indicate that hemodynamically important valvular regurgitation can result from suture perforations. This observation is in accord with previous experience with this problem, which resulted in a second aortic valvular replacement in at least two
patients.': 2 The morphology of the areas of the inflow surface that were in contact with the elongated suture ends differed from that seen in other types of perforations and tears that have been described in bioprostheses implanted in patients.'? Perforations associated with infection are much more irregular and contain abundant fibrin and inflammatory cells. Tears and perforations related to mechanical stresses in localized regions of the cusps also have fragmented ends of collagen on their surfaces (and also may be associated with calcific deposits). However, in our experience the latter lesions lack the crater-like appearance, with the broader end on the inflow surface, and the relatively even distribution of the collagen erosion that we observed in suture-induced perforations in bioprostheses implanted in the mitral position. The conclusions of this study are summarized as follows: (I) Cuspal perforations can be induced by excessively long suture ends in bioprostheses implanted in the mitral as well as in the aortic position; (2) such damage can occur both in pericardial and in porcine aortic valvular bioprostheses; (3) the lesions are morphologically characterized by a crater-like appearance, with the broader end of the crater adjacent to the elongated suture end; (4) the resulting lesions can be hemodynamically significant; and (5) care must be taken not to leave excessively long suture ends during implantation of bioprosthetic valves.
Addendum A recent bulletin from American Edwards Laboratories (Carpentier-Edwards Bioprostheses Clinical Report, January, 1985, 272-10/84-CV) has reported a total of 80 suture-related
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abrasions. Seventy-seven of these valves had been implanted in the aortic position and the other three in the mitral position. Therefore, these abrasions are more common than was previously thought to be the case. 6 REFERENCES
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