Stress Sharing Between the Sinus and Leaflets of Canine Aortic Valve

Stress Sharing Between the Sinus and Leaflets of Canine Aortic Valve Mano J. Thubrikar, Ph.D., Stanton P. Nolan, M.D., Jaafar Aouad, D.V.M., and J. David Deck, M.D. ABSTRACT A knowledge of the behavior of the aortic valve sinuses is necessary to the understanding of stress sharing between the sinuses and the leaflets. Radiopaque markers were placed on the sinuses and the leaflets of dogs during cardiopulmonary bypass, and the movement of the markers was studied using fluoroscopy. The center of the sinus moved radially during each cardiac cycle, but in an inconsistent manner. The sinus was under a dual influence: the passive influence of aortic pressure and the active influence of myocardial contraction. The longitudinal curvature of the sinus showed no dimensional change, whereas the radius of the circumferential curvature decreased by 15.7% from systole to diastole. In diastole, the stress in the sinus was 6.1 g/mm and was 24.3 g/mm circumferentially and 12.1 g/mm radially in the leaflet. Histologically, the main stress-bearing component of the leaflet was made up of thick, dense, collagenous fibers oriented circumferentially. These fibers curved into the sinus wall instead of inserting straight into the aortic wall, thereby suggesting that the high stress in the leaflet is shared with the sinus and that continuity of the circumferential stress exists between the leaflet and the sinus. The leaflet does not pull inwardly on the aortic wall. In diastole, the sinus adapts to the new stress conditions in the leaflet by reducing its radius of circumferential curvature. This stress sharing is important for the longevity of the aortic valve. valves, there are essentially no sinuses. When such a valve is implanted, the sinuses of the recipient are not connected to the leaflets of the bioprosthesis. Some bioprostheses subsequently have shown inward bending (permanent creep), probably because the load from the leaflet is transferred directly to the stent posts [lo- 121. The question then is how the leaflets in the normal valve are supported from the aortic wall. The present study investigates how stress is shared between the leaflets and the aortic sinuses. Material and Methods We investigated the functional changes in the normal geometry of canine (adult male or female mongrel dogs, 20-30 kg) aortic valve sinuses in vivo by using the marker-fluoroscopy technique that we described previously [13, 141. Radiopaque markers (platinum, 1 mm X 1 mm, 10 mg) were placed on the aortic valves in 7 dogs during cardiopulmonary bypass surgery. The markers were placed at the center of the valve sinuses in 3 dogs to determine displacement of these points during a cardiac cycle (Fig 1 I, 11). Two additional markers were placed at the center of the free edge of the two leaflets to I II The aortic sinuses of Valsalva are thought to play an important part in the hemodynamics of the aortic valve. Bellhouse and Talbot [l] and others [2-41 suggested that vortex formation in the aortic sinus is necessary for the closure of the valve leaflets. Bellhouse and colleagues [5] also suggested that the shape of the sinuses is important but less critical for valve closure. However, the role of the sinuses in the mechanics of the aortic valve is unexplored. In congenitally malformed valves (e.g., the unileaflet or bileaflet valve), the geometric relationship between the leaflet and the sinus is distorted. These valves are known to become diseased much more frequently than normal trileaflet valves [6-91. In bioprosthetic From the Departments of Surgery and Anatomy, University of Virginia Medical Center, Charlottesville, VA. Accepted for publication Jan 10, 1986. Address reprint requests to Dr. Thubrikar, Box 263, Department of Surgery, University of Virginia Medical Center, Charlottesville, VA 22908. Fig 2. Marker placement in the aortic valve. (1) Three markers-a, 3, and C-are at the center of the aortic sinuses. (11) Top view of the valve. Markers D and E are at the center of the free edge of two leaflets. (111, 1V) Markers R, M, and S indicate sinus curvature along the long axis of the aorta (longitudinal curvature). Markers L, M, and N show sinus curvature along the short axis of the aorta (circumferential curvature). The distances RMS and RS represent arc length and height, respectively, for the longitudinal curvature. The distances LMN and LN represent arc length and height (or width), respectively, for the circumferential curvature. Marker T is in the opposite commissure, and marker P is on the free edge of a leaflet. IV 434 Ann Thorac Surg 42:434-440, Oct 1986

435 Thubrikar, Nolan, Aouad, Deck Stress Sharing in Canine Sinus Leaflets LEAFLET SEPARATION I 0 - (mm) PERIMETER AORTIC PRESSURE 125 (mm Hg) 100 Fig 2. Leaflet separation, sinus perimeter, and aortic pressure plotted against time. Leaflet separation was measured as the distance between two leaflet markers (D and E in Figure I), indicating an open or closed valve. Each of the data points on the top two graphs is from a single video field. SINUS PERIMETER AT NORMAL AND HIGH BP SINUS PERIMETER AT LOW BP wn 5M 100136 53 F 146/137 1351102 75v 94-t III 72/50 1801146 Fig 3. Typical plots of the sinus perimeter at various systemic blood pressures (BP) in a single dog. The roman numerals I, 11, and 111 represent three studies performed at different times. The perimeter changes consistently at low pressures, but not at normal or high pressures. determine whether the valve was open or closed. Five markers were placed in the shape of a cross in one sinus in each of the remaining 4 dogs (Fig 1 I11 and IV). In this sinus, three markers (R, M, and S) indicated the sinus curvature along the long axis of the aorta (longitudinal curvature) and three markers (L, M, and N) indicated the curvature along the short axis of the aorta (circumferential curvature). One additional marker (T) was placed in the opposite commissure for valve alignment during fluoroscopy. To determine when the valve was open or closed, a marker (P) was placed at the center of the free edge of one leaflet. The dogs were allowed to recover and were then studied. During each study, the dogs were anesthetized and positioned under an image intensifier, and the movements of the markers were recorded on videotape at 60 fieldskec. The marker movement was recorded in both top and side views of the aortic valve, which were obtained by adjusting the dog or the x-ray tube, or both, so as to permit direct measurements of various parameters. Simultaneous with the fluoroscopic recordings, aortic pressure was recorded with a 7F catheter and Statham pressure transducer (model P23ID). The recordings of marker movements were repeated at higher and lower systemic pressures obtained by the intravenous infusion of angiotensin or nitroprusside, respectively. In general,

436 The Annals of Thoracic Surgery Vol 42 No 4 October 1986 - t 70- - E 76- E g 74- + g 72- [L W a 70- m 3 z 68- m 0 0 I " 0 0 0.. L 0 o SYSTOLIC DIASTOLIC 66l I 1 I I ' I I 20 60 100 140 180 220 AORTIC PRESSURE (rnrnhg) - Fig 4. Typical plot of the sinus perimeter versus the aortic pressure in a single dog. 17.5....-.'.-... - ' 12.5 Fig 5. Parameters of longitudinal curvature plotted against time. (H = height; distance RS in Figure 1.) each dog was studied at least twice, eight days and two to four weeks postoperatively. To analyze the marker movement, the videotape was displayed on a television screen in a stop mode and the marker positions were noted on transparent paper. The tape was advanced field by field for three cardiac cycles, and the marker positions were noted in each field. Fig 6. Parameters of circumferential curvature versus time. (H = height; distance LN in Figure I.) ARC LENGTH (mm) SYSTOLE^ - -.. 0 Silicone rubber casts of the aortic root were made in vitro at a diastolic pressure of 80 to 100 mm Hg in order to determine the radii of the sinuses along the directions of the markers and the radius of the leaflet in its circumferential direction. Sinus and leaflet thicknesses were also measured. Stresses in the sinus and in the leaflet were calculated during diastole, using these parameters. To examine the structure of the sinus-leaflet assembly, two additional dog roots were fixed with 2% glutaraldehyde at diastolic pressure and sectioned in an oblique plane, which passes through the circumferentially oriented collagen fibers of the leaflet. These sections were stained with hematoxylin and eosin for light microscopic examination. Results The centers of the sinuses did show a displacement in vivo during a cardiac cycle. The perimeter of an imaginary triangle, formed by three sinus markers (A, B, and C in Figure li), increased in systole and decreased in diastole (Fig 2). Detailed examination, however, showed that this behavior of the sinus was inconsistent at normal pressures and at high pressures (Fig 3). At lower pressures, the behavior of the center of the sinuses not only became consistent, but also was similar to the previously reported behavior of the base of the valve [15]. For instance, the sinus perimeter was at its maximum in early systole, decreased during systole, and began increasing again during diastole (see Fig 3), just as the base perimeter does [15]. Hence, the sinus appears to be under the combined influence of two factors that produce opposite effects: (1) the passive response of the aorta to the aortic pressure and (2) the active response of the base of the valve to ventricular contraction. In systole, increased pressure increases the diameter at the level of the commissures and the active contraction of the left ventricle reduces the diameter at the base of the leaflets. The sinus, lying between these two levels, is affected by both; the net result is governed by the RADIUS (rnm) WIDTH (mm) H

437 Thubrikar, Nolan, Aouad, Deck: Stress Sharing in Canine Sinus Leaflets RADIUS 120198 BP Fig 7. Typical plot of the parameters of circumferential curvature versus time for a single dog at various systemic pressures. The roman numerals I and II represent two studies at different times. (BP = blood pressure.) Decrease in the Parameters of Circumferential Curvature of the Sinus Bp Percentage Decrease" Aortic Pressure Width Dog No. (mm Hg) Arc Radius (height) 1 135180 7.6 14.6 12.6 144182 7.8 17.4 10.8 152'120 0 15.6 6.3 2251185 0 11.1 7.5 150/120 2.9 16.7 8.8 10488 0 14.3 7.0 2 1531130 0 14.3-1551133 5.9 15.8-8516.5 5.6 15.1 9.3 3 1681150 6.3 20 10.5 1881165 8.6 22.9 11.8 1401130 4.9 21.4 8.9 1551135 0 19.5 8.4 4 102160 3.9 12.6 13.2 1511122 2.5 12 12.2 158/118 3.2 10.4 12.6 88/59 6.2 13.3 15.5 Mean f SD 3.8 -+ 3 15.7 f 4 10.3 i 3 Tercentage decrease = (systolic - diasto1ic)lsystolic x 100% dominating factor, whichever it may be. During diastole, a decrease in the diameter at the commissural level and an increase in the diameter at the base also produce opposite effects on the sinus. Overall, the sinus perimeter does increase with aortic pressure (Fig 4). The curvatures of the sinus were measured in terms of the arc length, the radius, and the height (cord length) of an imaginary circle passing through three sinus markers. The longitudinal curvature of the sinus showed no change during a cardiac cycle (Fig 5). It seems that the sinus along the long axis of the aorta may rock back and forth, or move up and down as a whole, but it does not change its internal dimensions. The circumferential curvature of the sinus showed the most marked changes. All of the parameters-arc length, radius, and height (or width)-changed during a cardiac cycle (Fig 6), reaching their maximum in systole and their minimum in diastole. This qualitative change in circumferential curvature occurred at low, normal, or high systemic pressures (Fig 7>. The considerable change occurred in the radius of curvature, which decreased by an average of 15.7%. This change was associated with a mean decrease in arc length of 3.8% and a mean decrease in width of 10.3% (Table). The geometry of the sinus-leaflet assembly is complex, and stress determination is therefore quite complicated. The present study assessed the stresses approximately, using a simplified approach for stress determination. As observed from silicone rubber casts, the shape of the sinus in diastole was approximately spherical; in the load-bearing portion, the shape of the leaflet was cylindrical. If both the sinus and leaflet are considered thin shells, the stress in diastole was 6.1 g/mm2 in the sinus, 24.3 g/mm2 in the leaflet in the circumferential direction, and 12.1 g/mm2 in the leaflet in the radial direction (Fig STRESS IN THE SINUS: Spherical Shape PR uc = UL = - = 6.07 gms/mm' 2t For P = 100 mmhg, t = lmm, R = 9 mm. STRESS IN THE LEAFLET: Cylindrical Shape PR uc =-= 24.3 gms/mmz t PR and UL=-= 12.15 gms/mmz 2t for P = 100 mmhg, t = 0.5mm, R = 9 mm. Fig 8. Stress determination in the sinus and the leaflet. (uc and ul = stress in the circumferential and longitudinal [radial] direction, respectively. P, t, and R = the pressure gradient across the leaflet, the thickness, and the radius, respectively.)

438 The Annals of Thoracic Surgery Vol 42 No 4 October 1986 Fig 9. Oblique sections of the leaflet-sinus assembly. ( I ) Leaflet (L) attaches to the sinus wall ( S ) in such a way that the lamina fibrosa (F) of the leaflet runs along the inside of the sinus wall. (H& ; x 18.) (ZZ) Enlargement of the section shown in I at the leaflet attachment. A triangular wedge-shaped area is seen at the attachment. (G = loose, spongy tissue in this area; FE = fibroelastic lamina; F = lamina fibrosa.) (Ha ;X 60.) (111) A section farther up in the sinus uiall. Lamina fibrosa (F) of the leaflet interdigitates with alternating elastic and muscular layers of the sinus wall in an area indicated by the circle. (Ha ;x 60.) 8). A decrease in the radius of the circumferential curvature of the sinus, from systole to diastole, indicates that high stress in the circumferential direction of the leaflet is shared between the sinus and the leaflet, rather than the stress being transmitted to the intercommissural trigone. Examination of the structure of the valve showed that the three leaflets are attached to the aortic wall along a scalloped line, each leaflet partially enclosing an aortic sinus. Histological examination of the valve suggested that the principal stress-bearing tissue of the leaflets is the relatively thick, dense, collagenous layer of fibers beneath the aortic surface known as the lamina fibrosa. Most of the fibers of this layer are aligned with the free edge of the leaflet, which is attached to the wall at an angle of approximately 125 degrees. Therefore, fibers

439 Thubrikar, Nolan, Aouad, Deck: Stress Sharing in Canine Sinus Leaflets pass upward into the wall at a similar angle, as the oblique sections parallel to the free edge demonstrate (Fig 9). These sections also show that, except at the leaflet commissures, the lamina fibrosa of an individual leaflet curves into the wall of the aortic sinus instead of inserting straight into the intercommissural trigone (see Fig 9). Collagenous fibers from the leaflet fibrosa interdigitate in the sinus with the alternating elastic and muscular layers of the wall. Where the leaflet joins the wall, a region of loose, spongy tissue beneath the lamina fibrosa appears to act as a shock absorber. On the ventricular side, a very thin fibroelastic lamina attaches the underside of the leaflet to the wall of the ventricular outflow tract to facilitate the systolic flow of blood. It appears unlikely, however, that this thin layer bears a major degree of leaflet stress. Instead, the microscopic structure of the valve indicates that individual leaflets are suspended almost totally from their respective sinuses by means of the lamina fibrosa. C D Fig 10. Schematic drawings showing the presence or absence of stress sharing between the leaflet and the sinus. (A, B) Stress continuity exists between the leaflet and the sinus in the circumferential direction. The leaflet does not pull on the aortic wall. (C, D) For dilated sinus, stress sharing between the leaflet and the sinus is disturbed. The leaflet may pull on the wall. (E) In a bioprosthetic aortic valve, the leaflets exert an inward pull on the stent posts. E Comment The Leaflet-Sinus Assembly as a Unit The present study defined the structure-function relationship of the leaflet-sinus assembly. The center of the sinus is displaced outward as a response to increasing aortic pressure (see Fig 4). The most important change, however, occurs in the circumferential curvature of the sinus. In each cardiac cycle, the radius of curvature decreases from systole to diastole by 15.7% L 4% (see Fig 6; Table). This decrease in the radius of curvature occurs primarily as a result of a 10.3% decrease in the width of the circumferential curvature (see the Table) and indicates an inward bending of the sinus circumferentially in response to the leaflet stress in diastole. The leaflet has much greater (almost four times greater) stress circumferentially than the sinus (see Fig 9). This stress has to be either shared with the sinus or transmitted directly to the wall in the intercommissural trigone in such a way that it will pull the wall inward. The decrease in the radius of the circumferential curvature of the sinus indicates that the sinus adapts its geometry so that the stress is shared between the sinus and the leaflet. The stressbearing fibers (lamina fibrosa) of the leaflet curve inward along the sinus wall and become part of the sinus wall, rather than insert straight into the aortic wall (see Fig 9). Therefore, the stress is distributed in the leaflet-sinus assembly as if a circumferential continuity exists between the leaflet and the sinus (Fig 10A) and the leaflet does not pull on the wall between the sinuses (Fig 10B). Continuity between the geometry of the leaflet and the sinus in the circumferential direction was also observed by Swanson and Clark [16]. These observations demonstrate an important role of the aortic sinuses in valve mechanics. In diastole, the geometry of the sinus adapts so that the sinus and the leaflet together become an enclosed, self-sustained unit to contain the pressure within. This stress sharing prevents the concentration of stress at any given point and is important for the longevity of the natural valve. Malformed Valves and Bioprostheses In the dilated sinus (Fig loc, D) or in a bileaflet or unileaflet valve, the stress sharing between the leaflet and sinus will be disturbed, which may predispose these valves to pathologic changes. It is known that bileaflet and unileaflet valves become diseased much more frequently than trileaflet valves [6-91. The shape of the sinus is also important for proper stress sharing between the sinus and the leaflet. In bioprosthetic aortic valves, leaflet stress is transmitted directly to the stent posts, which results in an inward pull on the posts and can cause inward bending of the posts, as observed for some flexible stent bioprostheses [lo-121. Leaflet Stress We have previously observed that the intercommissural distance in the aortic valve changes as a function of leaflet stress [17]. In a closed valve, as ventricular pressure increases in early systole, the pressure gradient across the leaflet decreases. Therefore, stress in the leaflet decreases, and the commissures move outward. Conversely, as stress in the leaflet increases from systole to diastole, the commissures move inward. Because the commissures are the outer boundaries of the sinus itself, it is to be expected that the radius of circumferential sinus curvature will also decrease from systole to diastole, as was observed in the present study. The release of leaflet stress in early systole results in an increase in the radius of circumferential sinus curvature and an increase of the intercommissural distance, so that the latter then participates in the opening of the aortic valve [16]. References 1. Bellhouse BJ, Talbot L: The fluid mechanics of the aortic valve. J Fluid Mech 35:721, 1969 2. Lee CSF, Talbot L: A fluid-mechanical study of the closure of heart valves. J Fluid Mech 91:41, 1979 3. Peskin CS, Wolfe AW: The aortic sinus vortex. Fed Proc 37:2784, 1978

440 The Annals of Thoracic Surgery Vol 42 No 4 October 1986 4. van Steenhoven AA, van Dongen MEH: Model studies of the closing behaviour of the aortic valve. J Fluid Mech 90:21, 1979 5. Bellhouse BJ, Bellhouse F, Abbott JA, Talbot L: Mechanism of valvular incompetence in aortic sinus dilatation. Cardiovasc Res 7490, 1973 6. Campbell M: Calcific aortic stenosis and congenital bicuspid aortic valves. Br Heart J 30:606, 1968 7. Roberts WC: Anatomically isolated aortic valvular disease: the case against its being of rheumatic etiology. Am J Med 49:151, 1970 8. Fenoglio JJ Jr, McAllister HA Jr, DeCastro CM, et al: Congenital bicuspid aortic valve after age 30. Am J Cardiol 39:164, 1977 9. Thubrikar MJ, Aouad J, Nolan SP: Patterns of calcific deposits in operatively excised stenotic or purely regurgitant aortic valves. Am J Cardiol (in press) 10. Borkon AM, McIntosh CL, Jones M, et al: Inward stent-post bending of a porcine bioprosthesis in the mitral position: cause of bioprosthetic dysfunction. J Thorac Cardiovasc Surg 83:105, 1982 11. Salomon NW, Copeland JG, Goldman S, Larson DF: Unusual complication of the Hancock porcine heterograft: strut compression in the aortic root. J Thorac Cardiovasc Surg 77:294, 1979 12. Thubrikar MJ, Deck JD, Aouad J, Nolan SP: Role of mechanical stress in calcification of aortic bioprosthetic valves. J Thorac Cardiovasc Surg 86:115, 1983 13. Thubrikar M, Harry R, Nolan SP: Normal aortic valve function in dogs. Am J Cardiol 40:563, 1977 14. Thubrikar M, Piepgrass WC, Bosher LP, Nolan SP: The elastic modulus of canine aortic valve leaflets in vivo and in vitro. Circ Res 47:792, 1980 15. Thubrikar M, Nolan SP, Bosher LP, Deck JD: The cyclic changes and structure of the base of the aortic valve. Am Heart J 99:217, 1980 16. Swanson WM, Clark RE: Dimensions and geometric relationships of the human aortic valve as a function of pressure. Circ Res 35:871, 1974 17. Thubrikar M, Bosher LP, Nolan SP: Mechanism of opening of the aortic valve (letter to the editor). J Thorac Cardiovasc Surg 79:473, 1980