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J Thorac Cardiovasc Surg 2007;134:1562-1568
© 2007 The American Association for Thoracic Surgery

Surgery for Acquired Cardiovascular Disease

A saddle-shaped annulus reduces systolic strain on the central region of the mitral valve anterior leaflet

^a Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Ga
^b Harrison Department of Surgical Research, University of Pennsylvania School of Medicine, Philadelphia, Pa
^c Department of Mechanical Engineering, Texas Tech University, Lubbock, Tex
^d Engineered Tissue Mechanics Laboratory, Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pa.

Received for publication February 13, 2007; revisions received August 1, 2007; accepted for publication August 14, 2007.

^_* Address for reprints: Ajit P. Yoganathan, School of Biomedical Engineering, Suite 1126, IBB Building, 313 Ferst Dr, Georgia Institute of Technology, Atlanta, GA 30332-0535 (Email: ajit.yoganathan{at}bme.gatech.edu).

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion Conclusions References

 
Objectives: Mitral valve repair for degenerative diseases has shown suboptimal results in selected patients. Improved postinterventional mitral valve mechanics are essential to increase repair durability.

Methods: Eight porcine mitral valves were tested in a physiologic left heart simulator under normal hemodynamic conditions. Leaflet strain was measured by tracking the displacement of a 5 x 8 marker array located on the central region of the anterior leaflet. Local leaflet strain and strain rates were calculated from measured displacements. The experiments were conducted in 4 different annular configurations associated with saddle height/commissural diameter ratios of 0%, 10%, 20%, and 30%. All experiments were conducted in the normal papillary muscle position.

Results: For all annular configurations, the anterior leaflet material showed anisotropy, with the major principal strain in the radial direction and the minor principal strain in the circumferential direction. The peak major principal strain was 0.22 ± 0.07, whereas the peak minor principal strain was 0.11 ± 0.049 in the normal annular configuration (saddle height/commissural diameter ratio of 20%). The peak major principal strain was reduced by 13.52% ± 12.79%, 27.53% ± 13.65%, and 29.72% ± 29.79% for the 10%, 20%, and 30% saddle height/commissural diameter ratio configurations, respectively, when compared with reduction for the flat annular configuration. Peak strain in the circumferential direction was unaffected by annular curvature. Reduction in areal strain of 18.62% ± 18.98% and 27.97% ± 35.01% were observed for the 20% and 30% saddle height/commissural diameter ratio configurations, respectively.

Conclusion: The strain in the central region of the anterior leaflet is reduced with increasing annular saddle curvature. Decreased leaflet strain and associated stress might improve mitral valve repair durability.

	Introduction

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Because of the lower risk of complication, mitral valve (MV) repair is preferred over valve replacement for treatment of patients with mitral regurgitation.¹ Although the results for MV repair have improved during the past 3 decades,² recent long-term studies have shown repairs to be less durable than once thought.³ Improved postrepair mechanics of the MV are necessary to increase the efficacy and long-term durability of the initial repair.

Degenerative diseases of the MV, such as myxomatous degeneration, are commonly associated with abnormal tissue properties.^4,5 Changes to the microstructure of degenerative tissue lead to mitral leaflets and chordae tendineae with reduced strength and abnormal geometries. Therefore, in the case of degenerative disease, devising repair strategies and techniques that reduce stress on valve subcomponents might increase repair durability.⁶

Previous research in human subjects⁷ and animal models⁸ has shown that the native shape of the mitral annulus resembles a 3-dimensional saddle. Studies have also shown that the saddle shape of the mitral annulus might play a role in optimizing chordal force distribution⁹ and reducing leaflet stress.⁸ Salgo and colleagues⁸ proposed that saddle height/commissural diameter ratios (SRs) of greater than 20% were associated with minimum stress configuration for the central region of the anterior leaflet under systolic loading. Because of the absence of the subvalvular apparatus, the simplified geometry, and simplified material properties of the leaflets in this model, further research is warranted to demonstrate the effects of annular curvature on leaflet stress.

Stress cannot be measured directly on the leaflets of the MV under physiologic conditions. It can only be extrapolated on the basis of strain and a constitutive model. Therefore, the objective of this study is to measure the effect of annular saddle shape on leaflet strain in the central region of the anterior leaflet under physiologic conditions.

	Materials and Methods

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Mitral Valves
Eight fresh porcine MVs with similar orifice areas (6.8 ± 0.2 cm²) were obtained from the local abattoir. The valves were extracted from the hearts, preserving the complete mitral apparatus, including the papillary muscles (PMs).

In Vitro Flow Loop
The in vitro experiments were carried out in the modified Georgia Tech Left Heart Simulator (Figure 1, A). This system is capable of imposing physiologic and pathologic geometric and hemodynamic conditions on the MV. The ventricular chamber of this simulator has a traversing system to control the location of the PMs in 3-dimensional space. Additionally, force transducers attached to the PM positioning system allowed for the measurement of force on the individual PM. This simulator has been described in detail in previous studies.^10-13

View larger version (41K): [in this window] [in a new window]   Figure 1. A, Schematic of the Georgia Tech Physiological Left Heart Simulator and its different components. B, Diagram of the marker array used for the leaflet strain experiments. C, Dual-camera photogrammetric images of the mitral valve and the ink marker array.

Leaflet Strain Measurements
The marker technique was used to quantify leaflet strain under the different annular conditions. In this technique 2-dimensional images of miniature markers (Figure 1, B) on the valve leaflets from 2 synchronized high-speed cameras are used to obtain the 3-dimensional spatial coordinates of the markers by using a direct linear transformation. The strain distribution and principal strains are then computed for each frame of the cardiac cycle from these 3-dimensional coordinates of the markers.

Images of the markers from the 2 high-speed cameras (250 frames per second) were acquired as a sequence of TIFF files (Figure 1, C). The images from the frame grabber were synchronized, allowing simultaneous acquisition of images from the cameras and mitral flow and transmitral pressure information from the transducers in the left heart simulator. After image collection, a commercial digitizing software package was used to determine the x, y pixel coordinates of each of the markers in the region of interest from the sequential 2-dimensional images. A direct linear transformation method was used to reconstruct the 3-dimensional spatial coordinates from the recorded 2-dimensional images by using a calibration cube as the reference. Biquadratic finite element interpolation was used to fit a surface to the resulting 3-dimensional marker array.¹² The principal strains, areal strain, and principal angles were calculated for the center of the area of interest on the reconstructed surface.

The marker technique, its different steps, and the software used to calculate the strains on the anterior leaflet of the MV have been described in detail in previous publications.^12-14

Experimental Protocol
To use the marker technique to measure the strain on the anterior leaflet, an array of tissue dye (Thermo electron Corp) markers was used. A 5 x 8 (circumferential x radial) marker array was drawn on the center of the anterior leaflet (atrial surface), covering the whole radial distance from the annulus to 5 mm from the tip of the leaflet (Figure 1, B).

The atrial chamber containing the sutured MV was positioned in the left heart simulator. The PMs were attached to the force rods, and the left heart simulator was then filled with 0.9% saline solution. The high-speed cameras were placed in front of the left heart simulator facing the atrial chamber and focused on the atrial surface of the mitral leaflets (Figure 1, C). An in-house data collection program based on LabVIEW 5.0 software (LabVIEW, National Instruments Corp., Austin, Tex) was used to store the mitral flow and transmitral pressure information during the cardiac cycle. This software stored the curves representing 10 cardiac cycles for each variable. These curves were then averaged offline.

After preparing the system, the valve was placed in the defined normal PM position.¹⁵ The simulator was maintained under physiologic hemodynamic conditions (cardiac output, 5 L/min; peak transmitral pressure, 120 mm Hg; cardiac rate, 70 beats/min; systolic duration, approximately 300 ms). Hemodynamic data and images from the cameras were saved for offline processing.

After the initial set of recordings with the flat annulus (0% SR), experiments were repeated for SR configurations of 10%, 20%, and 30%. When changing the annular configuration, the PMs were relocated to maintain their normal position relative to the mitral annulus and avoid slack on the chordae tendineae. The relocation consisted of moving each individual PM apically until a similar PM force reading to that in the previous saddle configuration was observed. The lateral and posterior locations of the PMs were not varied between annular configurations.

Data Analysis
All data are reported as means ± 1 standard deviation unless otherwise stated. Percentage differences in principal strains and areal strains were calculated by using the flat annular configuration as the reference. The data for the major principal strain, minor principal strain, and areal strain were normally distributed. Analysis of variance (ANOVA) was used to determine whether SR had an effect on leaflet strains. Differences in strain for the different annular configurations were compared by using paired t tests. Statistical analysis was carried out with Minitab 14 (Minitab Inc) software.

	Results

Top Abstract Introduction Materials and Methods Results Discussion Conclusions References

 
Experiments were conducted on 8 MVs in the Georgia Tech Left Heart Simulator under physiologic pressure (transmitral pressure, 120 ± 2 mm Hg) and flow (cardiac output, 5.0 ± 0.2 L/min) conditions.

During systole, there was a rapid increase in strain, followed by a plateau that lasted approximately 200 ms (Figure 2). After the plateau, strain decreased with valve aperture (time >250 ms). The plateau corresponded to the maximum deformation of the tissue while the valves were closed and fully loaded. This behavior was observed in all of the studied valves for all annular configurations.

View larger version (38K): [in this window] [in a new window]   Figure 2. A, Plots of the major and minor principal strains during the systolic phase of the cardiac cycle for a typical porcine mitral valve. B, Average major and minor principal strains for the 8 valves studied during the systolic phase of the cardiac cycle. Bars represent 1 standard deviation.

The central region of the anterior leaflet was also characterized by a nonlinear load–strain response. The material response during the systolic loading phase is described in Figure 3. As shown, the stiffness of the leaflet increased with increasing transmitral pressure. Initially, strain increased linearly with transmitral pressure, allowing for large deformations at small increases in pressure. After 30% areal strain, there was a large increase in stiffness. Additionally, the loading and unloading strain curves for each of the valves did not follow the same path (Figure 3, B). Similar characteristics of anisotropy, nonlinear response, and differences in paths during loading and unloading were observed for all annular configurations.

View larger version (9K): [in this window] [in a new window]   Figure 3. A, Plot of transmitral pressure against average areal strain (n = 8) for the valves in the normal annular configuration. Error bars represent 1 standard deviation. B, Loading and unloading strain curves for typical mitral valve under physiologic conditions. Hysteresis is observed because the loading and unloading paths are different.

View larger version (38K): [in this window] [in a new window]   Figure 4. A, Average peak major principal strain for the different annular configurations. B, Average peak minor principal strain for the different annular configurations. C, Average peak areal strain for the different annular configurations. Paired t tests were used for statistical comparisons. Bars represent 1 standard deviation.

Variations in SR were also associated with changes in the areal strain on the central region of the anterior leaflet of the MV. As shown in Figure 4, C, there were significant reductions in areal strain for the 20% and 30% SR configurations when compared with those for the flat (0% SR) annular configuration. These reductions correspond to changes in areal strain of 18.62% ± 18.98% and 27.97% ± 35.01% for the 20% and 30% SR configurations, respectively. Although the 10% SR configuration appeared to induce a reduction in strain when compared with that of the flat annulus, this reduction was not statistically significant (P = .62).

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion Conclusions References

 
The marker technique has been used in previous studies to calculate the strain on the leaflets of the MV.^12-14 Previous in vitro^12,16,17 and in vivo¹⁴ studies have shown that MV leaflet material exhibits anisotropy, nonlinear load-strain relation, and hysteresis. As a result, these studies had characterized the material as viscoelastic. Further analysis of in vitro¹² and biaxial¹⁸ data demonstrated that although MV leaflet material exhibits the aforementioned characteristics, it does not exhibit creep or strain rate dependence and limited hysteresis for its response, and therefore this material should not be characterized as viscoelastic but rather as quasi-linear elastic.

This study concentrates on the central region of the anterior leaflet because Einstein and associates¹⁹ predicted that the peak principal stress on the MV leaflets occurred in this region during peak systolic loading. The results of the present study demonstrate that the central region of the anterior leaflet presented with anisotropy, nonlinearity, and hysteresis, which is in agreement with previous literature.¹² Anisotropy, increased circumferential stiffness, and nonlinear load–strain relationship are associated with collagen fiber orientation and crimping. In addition, the peak areal strain of 0.44 ± 0.14 (flat annulus) measured in the current study agrees well with the 0.47 peak areal strain obtained in a previous study¹² under similar conditions using a flat annular configuration. The systolic strain curves have similar loading characteristics as those observed in vivo, presenting rapid deformation rates followed by a stretch plateau.¹⁴ The peak strains in the current study were smaller than those observed in vivo in sheep, but these differences can be mostly attributed to methodological and interspecies variability.¹⁴ As shown in Figure 3, B, there was a large difference between the loading and unloading load–strain curves, which contrasts with previous research that showed limited hysteresis in mitral leaflet tissue.¹⁸ This difference can be attributed to variations in loading between the opening and closing phases, most likely associated with chordal forces and leaflet inertia.

The annular model used in these experiments maintains a constant 3-dimensional perimeter to avoid dilation of the valve while changing saddle curvature. The commissural sections of the annulus move apically to increase saddle curvature; the posterior annulus moves upward to maintain the 3-dimensional perimeter to compensate for this motion. Increasing saddle height while decreasing septal-lateral diameter are characteristics found in annular dynamics during changes in annular geometry from diastole to systole. Although the saddled annulus produced is smoother and more symmetric than that found in human subjects, its general characteristics are based on the normal human annulus.^6,20

As demonstrated by results from this study, there was a significant reduction in the areal strain in the central region of the anterior leaflet as a result of increasing saddle curvature. Most of the reduction in strain occurred in the radial direction. Because most of the collagen fibers in the central section of the anterior leaflet are arranged circumferentially, most of the physiologic deformation of the leaflet occurs radially.^12-14 Therefore, variations in leaflet strain caused by annular curvature might be more apparent in the radial direction. In contrast, the circumferential strain appeared to be less sensitive to saddle curvature. In the circumferential direction, peak strains were relatively small (between 7% and 11%) and therefore can be reached rapidly. Additionally, the constant commissural diameter for the different SR configurations and the symmetric insertion pattern of the chords severely restricted the circumferential curvature of the leaflets. The small strain range and the restrictions to circumferential leaflet curvature might both be responsible for the relative insensitivity of circumferential strain to saddle curvature.

Although this is the first experimental study that describes the relationship between leaflet strain and annular curvature, one computational study previously explored the relationship between saddle annular curvature and leaflet stress. Salgo and colleagues⁸ showed that both billowing and circumferential curvature, by themselves or in combination, reduced the stress on the mitral leaflets. At an SR of 20%, leaflet stress was reduced 3-fold (300%) to its minimum. The reduction in strain in this study is significantly less than the reduction in stress observed in the computational model.⁸

Biaxial studies of the central region of the anterior leaflet have shown that stress increases exponentially with increasing strain. Using these biaxial data¹⁸ and strain data from the current study, a decrease in stress of approximately 2-fold can be expected in the SR 20% configuration when compared with the stress in the flat annular configuration. The remaining differences between the studies are related to the methodologies but, more importantly, to the simplifications of the computational model.⁸ The absence of chordae tendineae in the computational model, which restrict leaflet curvature, and the use of a nonlinear material constitutive model, which does not account for tissue stiffening that decreases deformation, explain the larger reductions in stress observed in the computational model of Salgo and colleagues.⁸

As observed in the current study, increasing SR reduces the strain on the central region of the anterior leaflet. The areal strain is significantly reduced at SR configurations of 20% and greater. Therefore, a 20% SR configuration, which is the normal configuration of the mitral annulus, might be associated with a minimum threshold in curvature that can reduce leaflet strain and thus associated stress.

Although the change in the 2-dimensional projected area of the annulus might account in part for the reduction in strain with increasing saddle curvature, there are more significant factors to consider. If projected area was the only factor, both radial and circumferential strains should have been reduced. The reduction in strain with increasing saddle curvature might be explained by simple physical principles. For a cylindrical thin shell, Laplace’s law states that the surface tension is proportional to the pressure acting perpendicular to the surface and inversely proportional to surface curvature.²¹ Therefore, increasing saddle curvature should result in reduced tension and subsequent strain. Although Laplace’s law is associated with a simplified geometry, the thin-shell principle helps to explain how a saddle-shaped annulus can result in improved leaflet mechanics.

The left heart simulator has limitations, but it has been used successfully in several studies.^10-13 The marker technique has been validated to measure mitral leaflet strain both in vivo and in vitro.^12,13 Optical access is the major limitation associated with the marker technique because only discrete regions of the valve can be studied at a given time. In addition, because of the size of the data sets, strain measurements could only be acquired for a single cardiac cycle. Averaging over several cycles might provide more representative results. Although the annular model was designed to incorporate geometric characteristics associated with normal annular dynamics, further research on the effects of independent variations in commissural and septal-lateral diameter on leaflet strain is warranted because these variations are also associated to changes in saddle curvature. The present in vitro methodology provided good control over the variables of interest, and because this is a comparative study, the shortcomings of the model should not have a significant effect on the conclusions.

	Conclusions

Top Abstract Introduction Materials and Methods Results Discussion Conclusions References

 
The current study demonstrated that, independent of SR, the behavior of the central region of the anterior leaflet is highly anisotropic, with a nonlinear load–strain response. Although the MVs had similar overall responses to loading, the degree of deformation significantly varied for the different annular curvatures. There was a significant reduction in the areal strain in the central region of the anterior leaflet as a result of increasing saddle curvature. Most of the reduction in strain occurred in the radial direction. In contrast, the circumferential strain was less sensitive to saddle curvature.

Most repair failures in the setting of myxomatous disease are the result of disrupted suture lines or progressive chordal rupture. This implicates leaflet stress and the resulting strain as a contributing factor. Previous computational analysis has brought to light the potential benefits of maintaining leaflet curvature during valve repair.⁸ The data presented in this study strongly support the hypothesis that saddle shape annuloplasty might diminish leaflet strain and potentially increase repair durability.

	Footnotes

 
Supported by a grant from the National Heart, Lung, and Blood Institute (grant no. HL52009).

	References

Top Abstract Introduction Materials and Methods Results Discussion Conclusions References

 

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