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J Thorac Cardiovasc Surg 2004;128:543-551
© 2004 The American Association for Thoracic Surgery

Surgery for acquired cardiovascular disease

Functional mitral regurgitation in chronic ischemic coronary artery disease: Analysis of geometric alterations of mitral apparatus with magnetic resonance imaging

^a Department of Surgery, National Taiwan University Hospital, Taipei, Taiwan, ROC
^b Department of Medical Imaging, National Taiwan University Hospital, Taipei, Taiwan, ROC
^c Institute of Biomedical Engineering, National Taiwan University Medical College, Taipei, Taiwan, ROC
^d Center for Optoelectronic Biomedicine, National Taiwan University Medical College, Taipei, Taiwan, Republic of China

Received for publication December 13, 2003; revisions received March 31, 2004; accepted for publication April 6, 2004.

^* Address for reprints: Wen-Yih Isaac Tseng, MD, PhD, No. 1, Jen-Ai Road, Sec. 1, Center for Optoelectronic Biomedicine, National Taiwan University Medical College, Taipei, Taiwan, ROC
wytseng{at}ha.mc.ntu.edu.tw

	Abstract

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BACKGROUND: Patients with chronic coronary artery disease have double the mortality rate if the condition is combined with functional mitral regurgitation. An understanding based on geometric alterations of the mitral apparatus in functional mitral regurgitation is desirable.

METHODS: Twenty-nine subjects were enrolled in the study, including 9 healthy volunteers (control group), 12 patients with chronic coronary artery disease without functional mitral regurgitation (CAD group), and 8 patients with chronic coronary artery disease with functional mitral regurgitation (CAD+FMR group). Cine magnetic resonance imaging was performed to acquire multiple short-axis cine images from base to apex. Left ventricular end-systolic volume, left ventricular ejection fraction, mitral area, and vertices of the mitral tetrahedron, defined by medial and lateral papillary muscle roots and anterior and posterior mitral annulus, were determined from reconstructed images at end-systole. Anterior-posterior annular distance, interpapillary distance, and annular-papillary distance (the distance from the anterior or posterior mitral annulus to the medial or lateral papillary muscle roots) were calculated.

RESULTS: Left ventricular end-systolic volume was inversely associated with left ventricular ejection fraction (R² = 0.778). Left ventricular end-systolic volume was highly associated with distances related to ventricular geometry (R² = 0.742 for interpapillary distance, 0.792 for the distance from the anterior mitral annulus to the medial papillary muscle root, and 0.769 for distance from the anterior mitral annulus to the lateral papillary muscle root) but was moderately associated with distances related to annular geometry (R² = 0.458 for anterior-posterior annular distance and 0.594 for mitral area, respectively). Moreover, interpapillary distance of greater than 32 mm and distance from the anterior mitral annulus to the medial papillary muscle root of greater than 64 mm readily distinguished the CAD+FMR group from the other groups.

CONCLUSION: In patients with coronary artery disease, an increase in left ventricular end-systolic volume is associated with inadequate approximation of the mitral tetrahedron during systole, which consequently leads to functional mitral regurgitation. Our study suggests that interpapillary distance and distance from the anterior mitral annulus to the medial papillary muscle root are sensitive to the increase in left ventricular end-systolic volume and reliably indicate the presence of functional mitral regurgitation.

Dr Yu (left) and Dr Tseng (right)

Functional mitral regurgitation (FMR) caused by ischemia is found in 20% of patients with chronic coronary artery disease (CAD)¹ and in 59% of patients who present with poor left ventricular ejection fraction (LVEF). The mortality rate is doubled if chronic CAD is combined with FMR. Still, critical and effective treatments for FMR are lacking because of an inadequate understanding of the mechanism of this disease. In the present study geometric alterations of the mitral apparatus in patients with chronic CAD were characterized with magnetic resonance imaging (MRI). A mitral tetrahedron was defined by the medial and lateral papillary muscle roots and the anterior and posterior mitral annulus (Figure 1). The goal of the present study is to define the change in the mitral tetrahedron and its relationship with FMR.

View larger version (49K): [in this window] [in a new window]   Figure 1. Illustration of the mitral area and mitral tetrahedron. The mitral tetrahedron was determined by 4 vertices (A, anterior annulus; P, posterior annulus; M, medial papillary root; L, lateral papillary root) and 6 edges (DAM, distance between the anterior annulus and the root of the medial papillary muscle; DAL, distance between the anterior annulus and the root of the lateral papillary muscle; DPM, distance between the posterior annulus and the root of the medial papillary muscle; DPL, distance between the posterior annulus and the root of the lateral papillary muscle; DAP, distance between the anterior annulus and the posterior annulus; DML, distance between the roots of the medial and lateral papillary muscle.)

	Methods

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View larger version (38K): [in this window] [in a new window]   Figure 2. Cine MRI acquired in the left ventricular short-axis plane from base to apex. Gating acquisition was performed with prospective ECG R-wave triggers. Images at a temporal resolution of 30 ms and in-plane spatial resolution of approximately 1 x 1 mm2 were obtained. Cine images at end-diastole and end-systole are shown in the upper and lower rows, respectively.

Three-dimensional coordinates of the anterior and posterior annulus and medial and lateral papillary muscle roots were determined in the reconstructed long-axis views (Figure 3). These 4 points defined the 4 vertices of a tetrahedron, representing the geometry of the mitral apparatus. The lengths of 6 edges of the mitral tetrahedron at end-systole were calculated (Figure 1).

View larger version (69K): [in this window] [in a new window]   Figure 3. Interpolated and reconstructed images from original MRI data. Three-dimensional coordinates of the points of interest were determined on the long-axis planes decided from the lines of intersection on the short-axis plane. Left upper, Anterior annulus (denoted A and indicated with black arrow on the right panel) and posterior annulus (denoted P and indicated with white arrow). Left lower, Roots of the medial papillary muscle and the lateral papillary muscle (indicated with white dots). Right, Ten points along the mitral annulus (indicated with arrowheads). PL, Root of lateral papillary muscle; PM, root of medial papillary muscle.

Data analysis
Dichotomous data were compared by using the ² or Fisher exact tests. Numeric data were compared with the unpaired Student t test. Test of correlation between different variables was performed with a linear regression model. All statistical works were performed with SPSS for Windows (SPSS Inc).

	Results

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In the control, CAD, and CAD+FMR groups LVESV was 29.1 ± 17.0 mL, 60.3 ± 38.4 mL, and 183.4 ± 76.7 mL, respectively (P = .023 between the control and CAD groups and P < .001 between the CAD and CAD+FMR groups; Table 2), and LVEF was 0.65 ± 0.11, 0.50 ± 0.19, and 0.24 ± 0.10, respectively (P = .048 between the control and CAD groups and P = .002 between the CAD and CAD+FMR groups). On the basis of echocardiographic data, LVEF for the CAD+FMR group was less than that for the CAD group (0.37 ± 0.10 vs 0.57 ± 0.16, P = .006); LVEDD and LVESD for the CAD+FMR group was greater than that for the CAD group (58.3 ± 5.7 mm vs 51.0 ± 5.6 mm, P = .017, for LVEDD; 47.3 ± 5.9 mm vs 34.2 ± 8.6 mm, P = .003, for LVESD). The CAD+FMR group was associated with a higher percentage of right coronary artery involvement and old inferior infarction than the CAD group (87.5% vs 50.0%, P = .085, for right coronary artery lesion; 50% vs 16.7%, P = .111, for old inferior wall infarction).

Regression analysis was performed to define the relationship between the geometry of the mitral tetrahedron and LVESV (Figure 4). LVEF was found to be inversely correlated with LVESV (R² = 0.778). Different strengths of correlation were found between LVESV and the edge lengths of the mitral tetrahedron. Among the edge lengths in the longitudinal direction, the correlation was highest in D_AM and D_AL (R² = 0.792 and 0.769, respectively), followed by D_PM and D_PL (R² = 0.649 and 0.574, respectively). In the transverse dimension, the correlation was high in D_ML (R² = 0.742) but was moderate in D_AP and MA (R² = 0.458 and 0.594, respectively).

View larger version (24K): [in this window] [in a new window]   Figure 4. A, A scatter plot of the left ventricular end-systolic volume (LVESV) to the left ventricular ejection fraction (LVEF). B, Scatter plots of LVESV to each edge of the mitral tetrahedron and to the mitral area. X, Control group; open circle, CAD group; filled circle, CAD+FMR group. Horizontal lines indicate the cutoff values of respective parameters for FMR.

View larger version (13K): [in this window] [in a new window]   Figure 5. Scatter plots of 2 typical parameters of the ventricular factors (DML and DAM, left panel) and the annular factors (DAP and MA, right panel) for distinguishing the CAD+FMR group from the other groups. A clear distinction was found by using a DML of 32 mm and a DAM of 64 mm as thresholds.

	Discussion

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Ring annuloplasty is the most widely accepted surgical procedure for FMR in recent years. However, variable outcomes and a high rate of late recurrence have been reported.³ In addition, excessive downsizing of the circular ring can limit the dynamic motion of the mitral annulus or can cause complications of systolic anterior motion of the mitral anterior leaflet to obstruct the left ventricular outflow tract.⁴ The lack of effective treatment might be due to incomplete understanding of the pathophysiology of this complicated disease. Quantitative analysis of the mitral apparatus in patients with FMR, as presented in this study, provides information about geometric alteration of the apparatus during the process of FMR and helps clarify the effect of left ventricular dilation on each edge length of the mitral tetrahedron. On the basis of this knowledge, appropriate treatment methods could be developed.

Several study methods were used to investigate the pathophysiology of FMR, such as sonomicrometry crystal⁵ and radio-opaque marker placement^6-9 for animal studies and echocardiography for animal or human studies.¹⁰ Standard echocardiography can only retrieve 2-dimensional images, and it is difficult to translate that data into 3-dimensional information. Assessment of the mitral apparatus by means of 3-dimensional echocardiography has been reported recently,^11-13 but this method is time consuming and is not available for routine clinical use.¹⁴

Recent advance of the balanced steady state free precession sequence for cine MRI has shown the advantages of short acquisition time and good image quality.² For each slice location, it takes about 12 seconds to acquire cine MRI of approximately 30 time frames. It can be readily achieved in a breath hold, effectively suppressing the artifacts from respiratory artifacts. It usually requires 8 to 12 slices to cover the whole left ventricle. The total scan time was less than 10 minutes. All our patients could lie still in the magnet and performed multiple breath holds throughout the study. The only obvious contraindication is arrhythmia, which will degrade the image quality and make interpretation difficult. We did not encounter this situation in our subjects.

Many factors were proposed to account for FMR, such as dilation and sphericalization of the left ventricle,^15,16 altered leaflet tethering geometry,¹¹ annular dilation,¹⁷ and papillary muscle discoordination.¹⁸ Our study shows that ventricular factors, namely D_ML, D_AM, D_AL, D_PM, and D_PL, have stronger association with the LVESV than annular factors, namely, D_AP and MA (Figure 4, B). The lengthening of ventricular factors in systole can be attributed to general dilation of the left ventricle or to regional dyskinesia of the posterior wall. Among the ventricular factors, D_ML and D_AM are the most significant. All patients with FMR exclusively present with D_ML values of greater than 32 mm and D_AM values of greater than 64 mm, suggesting that these 2 edge lengths might be further lengthened during the process of FMR. If proved, these 2 parameters might serve as indicators for the assessment and treatment of FMR.

Our results showed that LVESV increased as LVEF decreased. This finding is compatible with the previous reports that left ventricular dilation occurs as an early response of decreased LVEF that is mandated to generate a normal stroke volume from a large ventricular end-diastolic volume.¹⁹ Because of strong association (R² = 0.742), we speculate that D_ML is sensitive to the increase of LVESV. The increase of D_ML theoretically pulls down the midpoints of the mitral leaflets (Figure 6, A), causing a predisposition toward central leakage. When the left ventricle dilates, its morphology changes from an ellipsoid to a spherical shape.^15,16 The increase of the width and diagonal of left ventricular geometry is disproportionately greater than the increase of the height. This explains our finding that the association between LVESV and D_AL or D_AM, representing the diagonal of the left ventricular geometry, was greater than that between LVESV and D_PL or D_PM, representing the height of the left ventricular geometry (Figure 4, B). In addition, the medial papillary muscle contributes more significantly than the lateral papillary muscle to the pathogenesis of FMR .^9,20,21 Therefore D_AM was found to have the highest correlation with LVESV. The increase of annular-papillary distance tethers the mitral leaflets (Figure 6, B), and if the tethering effect hinders the closure of the mitral leaflets, FMR occurs.

View larger version (35K): [in this window] [in a new window]   Figure 6. Illustration of the tethering effect by the structure of the mitral tetrahedron on the pathogenesis of FMR. A, Increased interpapillary muscle distance (DML) causes downward tethering of the midpoints of the mitral leaflets, a predisposition toward central leakage. B, When the increased annular-papillary distances are combined with increased anterior-posterior annular distance, the coapting points of the anterior and posterior leaflets (point C) were pulled apart. This causes FMR to happen.

To validate the data derived from MRI, we compared the results of the present study with those from animal studies using 3-dimensional echocardiography.^13,22 The body weight, LVESV, and MA of the control group in the experimental dogs were 20 to 28 kg, 17.1 ± 3.8 mL, and 5.5 ± 1.0 cm², and those of control group in the experimental sheep were 40 to 50 kg, 19.5 ± 1.6 mL, and 6.1 ± 0.3 cm², respectively. These data were in proportion to the data of the present study in which the body weight, LVESV, and MA in the control group were 50 to 76 kg, 29.1 ± 17.0 mL, and 9.2 ± 2.5 cm², respectively. One difference of the methodology in the present study from those seen in previous studies^13,22 is that papillary muscle roots, instead of the papillary muscle tips, were used as one end of the annular-papillary distance. This is because the papillary muscle tips usually branch (Figure 3), and therefore the bias of estimation can be reduced if the papillary muscle roots are measured.

Theoretically, revascularization of affected myocardium (usually the posterior wall of the left ventricle) is an ideal way to treat ischemic FMR. But for many cases, the chronic ischemic myocardium has become fibrotic scar and cannot be vitalized by means of revascularization. Therefore surgical correction for FMR on the basis of geometric consideration might play its role in these cases. Up to now, several novel surgical methods, focusing on either annular or subvalvular components,⁸ were developed to correct for FMR. The methods include ring annuloplasty, Paneth suture annuloplasty,²³ cutting of the basal chords to relieve leaflet retraction,²⁴ use of a ventricular containment device to restrain left ventricular dilation,²⁵ imbrication of interpapillary myocardium during ventricular restoration operation,²⁶ and use of a papillary sling to bring both papillary muscles into close contact.²⁷ Poor LVEF was often considered a risk factor for late recurrence of FMR in patients after ring annuloplasty.^3,28 We speculate that this might be related to annular-papillary distances that increase with LVESV and inversely with LVEF. As shown in our study, increased annular-papillary distances of D_ML and D_AM were found exclusively in the CAD+FMR group. However, this increase is not corrected for by the procedure of ring annuloplasty.

According to the findings of the present study, we propose that FMR can be treated more effectively by means of 2 alternative approaches: first, cephalic mobilization of the papillary muscle roots to decrease annular-papillary distances in systole, thus reducing the tethering effect on the mitral leaflets, and second, reduction of the anterior-posterior annular distance to restore the reserve of coaptation between both leaflets combined with reduction of interpapillary distance to relieve tethering on the midpoint of leaflets, thus preventing the corresponding central leakage. The first approach might be achieved by using a ventricular containment device, and the second approach by using ring annuloplasty plus either a papillary sling or imbrication of the interpapillary myocardium.

Limitations
The present study focused on a group of patients with chronic CAD disease. Whether the derived conclusion applies to FMR in the acute condition or other diseases requires further study. The differences of parameters between the CAD and CAD+MR groups can either be the cause or the results of FMR. For example, ventricular dilation can cause tethering of the mitral leaflets and FMR (type 3b). On the other hand, FMR can cause volume overload in the left ventricle and make it dilate. Our results suggest that, compared with annular factors, ventricular factors are more sensitive to the left ventricular dilation and that occurrence of FMR might aggravate the lengthening of D_ML and D_AM. The interplay between LVESV, mitral tetrahedron, and FMR awaits further investigation by applying the present MRI method to a group of patients with acute or subacute FMR. The CAD group and the CAD+MR group were not matched in many parameters, including LVEF, LVESV, and left ventricular end-diastolic volume, which confound the search for a single parameter as the sole culprit of FMR. Further study on more matched groups is warranted to study a single factor leading to FMR (eg, any specific edge of the mitral tetrahedron or MA). However, from the surgical point of view, the parameters gathered from preoperative MRI, as presented in this study, can provide surgeons with a useful guide to determine which part of the mitral tetrahedron and how much of it should be downsized for correction.

Although the horizontal spatial resolution was high (in-plane resolution of about 1 mm), the longitudinal resolution was relatively low (slice thickness of 10 mm) because of the requirement of reasonable examination time for the patients. Anatomic details, such as the mitral leaflets and chordae tendineae, cannot be delineated precisely in these images. The drawback of inadequate longitudinal resolution might compromise the accuracy of edge lengths in the longitudinal direction. Further development of faster cine MRI techniques or use of multidetector cardiac CT can provide more isotropic data for 3-dimensional reconstruction.

The effect of local ventricular function on papillary muscle motion and on annular contractility and their relationships to FMR were not investigated in this study.

Conclusions
This study introduces an MRI method to assess the geometry of the mitral apparatus in patients with chronic CAD with FMR. Alterations of edge lengths of the mitral tetrahedron can be determined for individual patients. According to the geometric information provided by using MRI, a surgical strategy can be custom designed.

	Acknowledgments

 
We thank Dr Jaw-Lin Wang for helpful discussions and Mr Riley Nick for technical assistance.

	Footnotes

 
This work was supported by the National Science Council, Taiwan (NSC91-2314-B-002-217-M08 and NSC93WFA0100159).

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