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Ann Thorac Surg 2003;76:1556-1563
© 2003 The Society of Thoracic Surgeons

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Original article: cardiovascular

Annuloplasty ring selection for chronic ischemic mitral regurgitation: lessons from the ovine model

^a Harrison Department of Surgical Research, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
^b Department of Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA

Accepted for publication May 20, 2003.

^* Address reprint requests to Dr Joseph H. Gorman, Department of Surgery, 6 Silverstein Pavilion, Hospital of the University of Pennsylvania, Philadelphia, PA 19104, USA
e-mail: gormanj{at}uphs.upenn.edu

	Abstract

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
BACKGROUND: Chronic ischemic mitral regurgitation (CIMR) is poorly understood and repair operations are often unsatisfactory. This study elucidates the mechanism of CIMR in an ovine model.

METHODS: Sonomicrometry array localization measured the three-dimensional geometry of the mitral annulus and subvalvular apparatus in five sheep before and 8 weeks after a posterior infarction of the left ventricle that produced progressive severe CIMR.

RESULTS: End systolic annular area increased from 647 ± 44 mm² to 1,094 ± 173 mm² (p = 0.01). Annular dilatation occurred equally along the anterior (47.0 ± 5.6 mm to 60.2 ± 4.9 mm, p = 0.001) and posterior (53.8 ± 3.1 mm to 68.5 ± 8.4 mm, p = 0.005) portions of the annulus. The tip of the anterior papillary muscle moved away from both the anterior and posterior commissures by 5.2 ± 3.2 mm (p = 0.021) and 7.3 ± 2.2 mm (p = 0.002), respectively. The distance from the tip of the posterior papillary muscle to the anterior commissure increased by 11.0 ± 5.7 mm (p = 0.032) while the distance from the tip of the posterior papillary muscle to the posterior commissure remained constant.

CONCLUSIONS: Progressive dilatation of both the anterior and posterior mitral annuli, increased annular area, and asymmetric ventricular dilatation combine to cause CIMR by distortion of mitral valve geometry and tethering of leaflet coaptation. Therefore complete ring annuloplasty may be superior to partial annuloplasty in the treatment of CIMR.

	Introduction

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Ischemic mitral regurgitation (MR), or "functional" MR secondary to postinfarction ventricular remodeling [1], continues to be a difficult clinical problem for surgeons. The results of reconstructive procedures for ischemic MR are unpredictable because of our poor understanding of the mechanisms that renders the valve incompetent [2]. Furthermore postoperative survival is consistently poor, typically 50% after 5 years, and debate continues as to whether repair is preferable to replacement [3–5]. While undersized ring annuloplasty relieves ischemic MR in many patients, the success and durability of this procedure can be unreliable in those who have complex MR jets and mild to moderate annular dilatation [5–7].

Our ignorance of the mechanisms responsible for ischemic MR has been reduced by work in experimental models of acute ischemic MR (AIMR) [8–11]. Using sonomicrometry array localization (SAL) [8–10], myocardial marker technology [11], and three-dimensional echocardiography [12] investigators have demonstrated that submillimeter distortions in the geometry of the annular and subvalvular apparatus can lead to severe MR in acute models. However in chronic ischemic MR (CIMR), valvular incompetence is usually mild early after the acute infarction but becomes progressively more severe as postinfarction ventricular remodeling occurs. The reason why these morphologically normal valves leak is often unclear and cannot be elucidated by two-dimensional echocardiography. Using SAL we now describe the geometric changes responsible for the development of CIMR in a well-established ovine model of the disease.

	Material and methods

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In compliance with guidelines for humane care (National Institutes of Health Publication No. 85-23, revised 1985) nine Dorsett hybrid sheep (35 to 45 kg) obtained from two University-approved vendors were intubated and anesthetized and ventilated with isofluorane (1.5% to 2%) and oxygen. The surface electrocardiogram and arterial blood pressure were monitored.

Through a sterile left lateral thoracotomy snares were placed around the proximal second and third obtuse marginal branches of the circumflex coronary artery (OM₂ and OM₃) [13]. Sixteen 2-mm hemispherical PZT-5A piezoelectric transducers (Crystal Biotech, Hopkinton, MA) were placed in each sheep before and during cardiopulmonary bypass as described previously [8, 14]. Three transducers on the chest wall defined a reference frame: two epicardial transducers defined the midventricular short axis and one marked the apex. Six transducers were placed around the mitral valve annulus. Figure 1 depicts the locations of the annular transducers. The posterior commissure (PC) and anterior commissure (AC) transducers were placed as close as possible to the cleft between the anterior and posterior leaflets. In all animals the AC transducer was very near the central fibrous body. The aortic crystal (Ao) was placed on the aortic-mitral continuity very near the posterior trigone. The annular transducers marked P1, P2, and P3 were centered over the anterior, middle, and posterior scallops of the mural leaflet. The remaining four transducers were sutured to the tips and bases of both papillary muscles.

View larger version (118K): [in this window] [in a new window]   Fig 1. The relationship of the sonomicrometry transducers, annular anatomy, coronary anatomy, and infarct location. The nomenclature for the transducers is as follows: anterior commissure (AC), aortic (AO), posterior commissure (PC), anterior portion of mural annulus (P1), mid portion of mural annulus (P2), and posterior portion of mural annulus (P3). The second and third obtuse marginal branches of the circumflex coronary artery, which are ligated in this model of chronic ischemic mitral regurgitation, are marked OM2 and OM3; and the posterior descending coronary artery is marked PDA. Note that transducers P2, P3, and PC are most closely associated with the infarct. Also note that AC and AO are closely related to the anterior and posterior trigones of the heart’s fibrous skeleton, respectively.

Subdiaphragmatic echocardiographic color flow Doppler velocity maps (E-CFDVM)—to assess the degree of mitral regurgitation (model 77020A, Hewlett-Packard)—were obtained through a sterile, upper midline laparotomy as previously described [15]. Mitral regurgitation was graded on a 0 to 4+ scale, where 0 represents no MR and 4+ represents severe MR with reversal of pulmonary vein flow. Transducer wires were connected to a Sonometrics Series 5001 digital sonomicrometer (Sonometrics, London, Ontario). Ventilation was suspended during sonomicrometry measurements. All 120 distances between 16 transducers were measured every 5 ms during a 5-s data run. The ECG, LV, and aortic root pressures were recorded simultaneously with the sonomicrometry data.

Coronary snares were exteriorized. Before infarction each animal was treated with a standardized pharmacologic protocol to prevent arrhythmias and maintain hemodynamic stability [16]. Snares, occluding OM₂ and OM₃, were sequentially pulled up over a 5-minute period. After the animal’s hemodynamics and ECG stabilized, the abdominal wound was closed and the animal was allowed to emerge from anesthesia.

After 8 weeks each animal was returned to the operating room and anesthetized. A second midline laparotomy was performed. Echocardiographic images were again obtained to evaluate MR and SAL data were acquired as described.

Animals were euthanized with 1 g thiopental and 80 mEq KCl. Hearts were removed and opened to verify the placement of the endocardial and epicardial sonomicrometry transducers.

Data analysis
As described previously [14], sonomicrometry distance data were used to determine the three-dimensional coordinates of each transducer every 5 ms throughout the cardiac cycle. To compare transducer movements and changes in chord lengths in each sheep before and 8 weeks after infarction (10 data sets), end diastole (ED), end isovolemic contraction (EIVC), end systole (ES), and end isovolemic relaxation (EIVR) time points were determined [14]. Every data set was then normalized in time by means of linear interpolation such that heart rate was 120 beats per minute, isovolemic contraction (from ED to EIVC) was 75 ms, ejection (EIVC to ES) was 220 ms, isovolemic relaxation (ES to EIVR) was 50 ms, and diastolic filling (EIVR to ED) was 155 ms. The normalized heart rate and cardiac cycle time divisions represent averages of all 10 data sets. Neither the average heart rate nor the degree to which each portion of the cardiac cycle was adjusted in the process of normalization was statistically different after infarction when compared with baseline.

Composite chord lengths were then calculated as the average of all five animals and plotted against time before and 8 weeks after infarction. Preinfarction and postinfarction chord lengths were compared by one-way analysis of variance ([ANOVA] entire cardiac cycle considered). If a particular chord was found to change significantly with infarction, that chord was evaluated at every time point in the cardiac cycle (every 5 ms) by paired Student’s t test. Error ranges are presented as standard deviations.

	Results

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Nine animals survived instrumentation and infarction. Of these nine, five developed severe MR (3+ or 4+) by the 8-week study and four had 1+ or less MR. These four animals were found to have only partial infarction of the posterior papillary muscle, which was partially supplied by the posterior descending coronary artery and which was not ligated in any animal. The data for the five sheep with MR at 8 weeks after infarct are presented.

The average changes throughout the cardiac cycle in selected key intraannular and annular-papillary muscle relationships are reported here. The associated ES measurements are summarized in Table 1. Hemodynamic data are summarized in Table 2.

View larger version (28K): [in this window] [in a new window]   Fig 2. Changes in annular area (A) and circumference (B) associated with chronic ischemic mitral regurgitation. Each graph represents an average of five animals. Changes in both annular area and annular circumference with infarction were significantly different by one-way analysis of variance (p < 0.05). Using paired Student t tests the preinfarct and postinfarct data were significantly different (p < 0.05) at every time point for both area and circumference. End diastole is defined as time = 0. (EIVC = end isovolemic contraction; EIVR = end isovolemic relaxation; ES = end systole.)

View larger version (41K): [in this window] [in a new window]   Fig 3. An illustration of the shape of the mitral annulus at end systole before (left) and 8 weeks after infarction (right). A surface passing through each of the annular transducers demonstrates the three-dimensional shape of the annulus. The technique used to construct the surface has been described previously [14]. The surface is not meant to represent the valve leaflets but is merely a device to allow a three-dimensional perspective. All sheep studied had annuli of similar shape. Note the degree of dilatation after infarction and the saddle shape of the mitral annulus. This animal had 3+ mitral regurgitation at 8 weeks after infarction. (AC = anterior commissure; AO = aortic; PC = posterior commissure; anterior (P1), mid (P2), and posterior (P3) portion of mural annulus.)

View larger version (17K): [in this window] [in a new window]   Fig 4. (A) Sonomicrometry array localization two-dimensional axial view (looking from the left atrium into the ventricle, as in Fig 1) of the mitral valve annulus and papillary muscle transducers before (solid lines) and 8 weeks after infarction (dashed lines). Note the stretching of both the posterior part of the aortic portion of the annulus (Ao to PC) and the anterior part of the mural portion of the annulus (AC to P1 to P2). Also, notice how the portion of the annulus between P2 and PC (along with the posterior papillary muscle tip [PPT]) is distracted away from the relatively fixed anterior commissure. (B) Two-dimensional sagittal view (as if looking at the heart though a left thoracotomy) of the sheep mitral annulus and its relationship to the left ventricle and papillary muscles before and 8 weeks after infarction. Note that both the anterior papillary muscle tip (APT) and the PPT are retracted away from the annulus. The mitral valve depicted in this figure is the same one shown in Figure 3. (AC = anterior commissure; AO = aortic; PC = posterior commissure; anterior (P1), mid (P2), and posterior (P3) portion of mural annulus.)

Annular-papillary muscle relationship
The changes in the average distance between the tip of each papillary muscle and each commissure due to postinfarction remodeling are presented in Figures 5 and 6. The ES values are summarized in Table 1 and the changes for a single representative animal are illustrated in Figure 4.

View larger version (28K): [in this window] [in a new window]   Fig 5. Changes in the relationship of the anterior papillary muscle tip (APT) to the (A) anterior commissure (AC) and the (B) posterior commissure (PC) associated with chronic ischemic mitral regurgitation. Each graph represents an average of five animals. Changes in both APT to AC and APT to PC with infarction were significantly different by one-way analysis of variance (p < 0.05). Using paired Student t tests, the preinfarct and postinfarct data were significantly different (p < 0.05) at every time point, for APT to AC and APT to PC. (EIVC = end isovolemic contraction; EIVR = end isovolemic relaxation; ES = end systole.)

View larger version (27K): [in this window] [in a new window]   Fig 6. Changes in the relationship of the posterior papillary muscle tip (PPT) to the (A) anterior commissure (AC) and the (B) posterior commissure (PC) associated with chronic ischemic mitral regurgitation. Each graph represents an average of five animals. Changes in both PPT to AC and PPT to PC with infarction were significantly different by one-way analysis of variance (p < 0.05). Using paired Student t tests, the preinfarct and postinfarct data were significantly different (p < 0.05) at every time point for PPT to AC, but not for PPT to PC. (EIVC = end isovolemic contraction; EIVR = end isovolemic relaxation; ES = end systole.)

The ES distance from the posterior papillary muscle tip (PPT) to the AC increased 31% from 35.3 ± 11.7 mm to 46.3 ± 7.9 (p = 0.032). Surprisingly the distance from the PPT to the PC did not significantly increase at any time point during systole (Fig 6, B).

	Comment

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Our previous work [8–10], which has been confirmed by others [11, 12, 17, 18], demonstrated that proper mitral valve function is dependent on a precise geometric coordination between the annulus and subvalvular apparatus during systole. These prior studies in an ovine model of AIMR, which infarcts 32% of the LV mass [10], demonstrated a surprising sensitivity of the valvular mechanism to geometric perturbations. Exceedingly small (1 to 3 mm) changes in the geometric relationship between the annulus and the subvalvular apparatus along with a discoordination in papillary muscle contraction contributed to gross valvular incompetence [8, 11]. The geometric changes reported in the present study of CIMR are much greater in magnitude; however in some instances the changes contradict current clinical impression.

End systolic annular area increased an average of 69% as a result of postinfarction remodeling. In most mammalian species the ratio of total area of mitral leaflet tissue to annular area at ES is between 1.5:1 and 2.0:1 [9, 19]. In sheep this ratio is 1.5:1 [10]. Therefore the degree of annular dilatation seen in this model likely contributed to valve incompetence but may or may not in human patients. The concept that annular dilatation is an important component of the mechanism leading to CIMR is well accepted clinically [2, 20, 21] but is not always apparent at operation.

The distribution of the dilation around the annulus in this model was unexpected. We found that all quadrants of the annulus dilated significantly but asymmetrically. It is a well-accepted concept among cardiac surgeons that the portion of annulus that supports the anterior leaflet is not susceptible to dilatation [22–25]. However we found that the anterior annulus dilated to the same extent as the posterior annulus. The segment between the anterior commissure transducer (AC in Fig 1) and the aortic transducer (Ao), which roughly approximates the intertrigonal distance, was found to dilate nearly 20%. Documentation that the fibrous cardiac skeleton can experience remodeling-induced dilatation is an important finding that has recently been suggested in a study of human pathologic specimens [26].

Interestingly the data indicate that portions of the annulus remote from the infarct stretch the most (AC-P1-P2 and Ao-PC). This is a striking example of how a localized moderately sized infarct can initiate a remodeling process that results in distortions at remote, fully perfused sites within the myocardium [27]. This phenomenon may be similar to the progressive myopathic process associated with ventricular remodeling which our group has described in other ovine models of congestive heart failure [27].

Another example of the global nature of the postinfarction remodeling process can be seen in the measured changes in the relationship between the papillary muscle tips and the commissures. The anterior papillary muscle tip was drawn away from both the anterior and posterior commissures to approximately the same degree (5.2 mm and 7.3 mm, respectively). Surprisingly the posterior papillary muscle maintained its relationship with the posterior commissure but moved an average of 11.0 mm farther from the anterior commissure.

These data are consistent with the idea that the infarcted posterior wall, papillary muscle, and annulus stretch, moving away from the anterior LV and distorting the entire ventricle. This study made no attempt to image the leaflets but the changes in the relationship of the papillary muscle tips to the commissures indicate that tethering of both the anterior and posterior leaflets likely contribute to the pathogenesis of CIMR.

This phenomenon is distinct from what we have described in our previous studies of AIMR. After acute infarctions that lead to MR in the ovine model there is a discoordination of the usually synchronized papillary muscle contraction. Comparison between the results of the present study and our previous studies indicate clearly that AIMR and CIMR are two distinct diseases. Chronic ischemic MR results from relatively large structural distortions of the entire annulus and LV as opposed to the minimal increase in annular area and subtle papillary muscle functional changes responsible for AIMR.

Our findings confirm some of the prevalent theories concerning the mechanism of CIMR, namely the association with annular dilation and posterior papillary muscle displacement [2–4, 20, 21]. However our data also contradict the commonly held belief that annular dilation is confined to the posterior or mural portion of the annulus and that only the posterior papillary muscle tethers the leaflets. Our findings if corroborated may alter surgical therapy for CIMR in several ways.

Currently undersized ring annuloplasty is the mainstay of surgical therapy for CIMR [28]. But there is a lack of agreement among surgeons regarding the type of annuloplasty ring that is best. Because the entire annulus can be distorted by a localized infarct, complete ring annuloplasty is probably superior to partial annuloplasty. Stabilizing the posterior annulus alone may restore valve competence acutely but continued progression of anterior annular distortion may predispose to recurrent MR as the ventricle continues to remodel.

Some authors have suggested that more lasting and effective repairs may be achieved by including maneuvers directed at reestablishing ventricular geometry and reducing leaflet tethering of a retracted posterior papillary muscle [29]. The list of suggested procedures has included pericardial restraint of the posterior wall [30], skeletal muscle myoplasty [31], infarct plication [32], posterior papillary muscle to posterior annular plication stitches [33], pericardial patch augmentation of the posterior leaflet, and even posterior wall excision [34]. This study indicates that the ventricular distortion and resulting leaflet tethering effects associated with CIMR are potentially far more complex than those caused simply by a retracted posterior papillary muscle. As a result these empirically designed repair techniques may prove ineffective or even detrimental.

Although the sheep model studied is very similar to human CIMR there are subtle differences in sheep mitral valve anatomy when compared with the human valve [14]. In spite of these anatomic differences the understanding of the ventricular remodeling process leading to CIMR gained from this model may be invaluable in developing strategies to treat or prevent the disease.

	Acknowledgments

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 
Supported by HL36308 and HL63954 from the National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, MD, and grants from the Mary L. Smith Charitable Trust and W. W. Smith Charitable Trust, both of Newtown Square, PA.The editor thanks Dr David Fullerton for managing the blinded peer review.

	References

Top Abstract Introduction Material and methods Results Comment Acknowledgments References

 

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				L. P. Ryan, B. M. Jackson, L. M. Parish, T. J. Plappert, M. G. St. John-Sutton, J. H. Gorman III, and R. C. Gorman Regional and Global Patterns of Annular Remodeling in Ischemic Mitral Regurgitation Ann. Thorac. Surg., August 1, 2007; 84(2): 553 - 559. [Abstract] [Full Text] [PDF]

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				Y. Enomoto, J. H. Gorman III, S. L. Moainie, B. M. Jackson, L. M. Parish, T. Plappert, A. Zeeshan, M. G. St. John-Sutton, and R. C. Gorman Early Ventricular Restraint After Myocardial Infarction: Extent of the Wrap Determines the Outcome of Remodeling Ann. Thorac. Surg., March 1, 2005; 79(3): 881 - 887. [Abstract] [Full Text] [PDF]

				Y. Enomoto, J. H. Gorman III, S. L. Moainie, T. S. Guy, B. M. Jackson, L. M. Parish, T. Plappert, A. Zeeshan, M. G. St. John-Sutton, and R. C. Gorman Surgical treatment of ischemic mitral regurgitation might not influence ventricular remodeling J. Thorac. Cardiovasc. Surg., March 1, 2005; 129(3): 504 - 511. [Abstract] [Full Text] [PDF]

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				J. H. Gorman III and R. C. Gorman Chronic Ischemic Mitral Regurgitation: Toward a Solution or Still an Enigma? Reply Ann. Thorac. Surg., February 1, 2005; 79(2): 752 - 753. [Full Text] [PDF]

				E. C. McGee Jr, A. M. Gillinov, E. H. Blackstone, J. Rajeswaran, G. Cohen, F. Najam, T. Shiota, J. F. Sabik, B. W. Lytle, P. M. McCarthy, et al. Recurrent mitral regurgitation after annuloplasty for functional ischemic mitral regurgitation J. Thorac. Cardiovasc. Surg., December 1, 2004; 128(6): 916 - 924. [Abstract] [Full Text] [PDF]

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				L. M. Parish, B. M. Jackson, Y. Enomoto, R. C. Gorman, and J. H. Gorman III The Dynamic Anterior Mitral Annulus Ann. Thorac. Surg., October 1, 2004; 78(4): 1248 - 1255. [Abstract] [Full Text] [PDF]

				S. A. de Oliveira Invited commentary Ann. Thorac. Surg., June 1, 2004; 77(6): 1988 - 1988. [Full Text] [PDF]

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