Influence of Anterior Mitral Leaflet Second-Order Chordae on Leaflet Dynamics and Valve Competence
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1 Influence of Anterior Mitral Leaflet Second-Order Chordae on Leaflet Dynamics and Valve Competence Tomasz A. Timek, MD, Sten Lyager Nielsen, MD, G. Randall Green, MD, Paul Dagum, MD, PhD, Ann F. Bolger, MD, George T. Daughters, MS, J. Michael Hasenkam, MD, Neil B. Ingels, Jr, PhD, and D. Craig Miller, MD Department of Cardiovascular and Thoracic Surgery and Division of Cardiovascular Medicine, Stanford University School of Medicine, Stanford, California, Department of Cardiothoracic and Vascular Surgery, Aarhus University, Aarhus, Denmark, and the Department of Cardiovascular Physiology and Biophysics, Research Institute of the Palo Alto Medical Foundation, Palo Alto, California Background. Chordal transposition is used in mitral valve repair, yet the effects of second-order chord transection on valve function have not been extensively studied. We evaluated leaflet coaptation, threedimensional anterior mitral valve leaflet shape, and valve competence after cutting anterior second-order chordae. Methods. In 8 sheep radiopaque markers were affixed to the left ventricle, mitral annulus, and leaflets. Animals were studied immediately with biplane videofluoroscopy and echocardiography before (Control) and after (Cut2) severing two anterior second-order strut chordae. Leaflet coaptation was assessed as separation between leaflet edge markers in the midleaflet and near each commissure (anterior commissure, posterior commissure). Anterior leaflet geometry was determined 100 milliseconds after end-diastole from three-dimensional coordinates of 13 markers. Results. Anterior leaflet geometry changed only slightly after chordal transection without inducing mitral regurgitation. Leaflet coaptation times were and milliseconds at the anterior commissure; 72 21, milliseconds at midleaflet, and and 75 8 milliseconds at the posterior commissure (p NS) for Control and Cut2, respectively. Conclusions. Cutting anterior second-order chordae did not cause delayed leaflet coaptation, alter leaflet shape, or create mitral regurgitation. These data indicate that transposition of second-order anterior chordae ( strut chordae) is not deleterious to anterior leaflet motion per se. (Ann Thorac Surg 2001;72:535 41) 2001 by The Society of Thoracic Surgeons Accepted for publication April 5, Address reprint requests to Dr Miller, Department of Cardiovascular and Thoracic Surgery, Falk Cardiovascular Research Center, Stanford University School of Medicine, Stanford, California ; dcm@stanford.edu. Mitral valve reconstruction provides durable and predictable results in certain forms of mitral regurgitation [1, 2], and reparative techniques continue to evolve to encompass a wider spectrum of mitral pathology, thereby extending the indications for repair [3, 4]. The more difficult problem of anterior leaflet prolapse has been repaired by transposing second-order chordae of the anterior mitral valve leaflet to the leading edge of the leaflet [5 7]. Transposition of either posterior leaflet or second-order anterior chordae to the anterior leaflet leading edge has been shown to provide superior results compared to chordal shortening [8]. Although chordal transposition has its advocates, the physiologic function of the anterior second-order chordae has not been clearly defined. Although the importance of mitral valve chordae tendineae in terms of preserving systolic left ventricular (LV) systolic function has been illustrated both experimentally and clinically [9, 10], these studies did not investigate the selective function of the first-order (or marginal chordae inserting on the leading edge) and second-order (which insert at the junction of the smooth and rough zones) anterior leaflet chordae. One recent experimental study suggested that the second-order chordae are predominantly responsible for valvular ventricular interaction (thereby optimizing LV systolic performance and geometry), whereas the first-order anterior chordae simply prevent leaflet prolapse and mitral regurgitation [11]. The above referenced experiment, however, was performed in an isolated working pig heart model that used load-dependent measures of anterior LV wall shortening and LV pump function; to date, no in vivo investigation of the influence of second-order chordae on leaflet function and valvular competence has been conducted. Hence, this experiment was designed to investigate the effects of cutting the second-order chordae of the anterior leaflet on mitral leaflet coaptation, valvular competence, and three-dimensional (3-D) leaflet shape by The Society of Thoracic Surgeons /01/$20.00 Published by Elsevier Science Inc PII S (01)
2 536 TIMEK ET AL Ann Thorac Surg ANTERIOR MITRAL LEAFLET SECOND-ORDER CHORDAE 2001;72: Fig 1. (A) Array of left ventricular markers and schematic representation of the coordinate system used for calculating marker threedimensional coordinates (APM anterior papillary muscle; PPM posterior papillary muscle). (B) Mitral annular and leaflet marker array with corresponding marker numbers. (AMVL anterior mitral valve leaflet; PML posterior mitral leaflet; ACOM anterior [or anterolateral] commissure; PCOM posterior [or posteromedial] commissure.) Material and Methods Surgical Preparation Eight adult male sheep were used in the study. The radiopaque marker techniques used have been described previously [12], and only details specific to this experiment will be presented. Eight subepicardial tantalum helices (inner diameter, 0.8 mm; outer diameter, 1.3 mm; length, 1.5 to 3.0 mm) were inserted along four equally spaced LV longitudinal meridians at two levels between LV apex and base (Fig 1A). After establishment of cardiopulmonary bypass and cardioplegic arrest, eight miniature markers were sutured equidistantly (approximately every 45 ) around the circumference of the mitral annulus (one near each commissure and three along the anterior and posterior annulus, markers 14 to 21) as shown in Figure 1B. Three leaflet markers were sutured equidistantly along the anterior (markers 31, 27, and 24) and posterior (markers 32, 28, and 25) leaflet edges with three additional markers being placed on the anterior leaflet closer to the annulus (markers 29, 26, and 22). Subsequently, the largest of the multiple second-order chordae emanating from each papillary muscle and leading to the central portion of the anterior leaflet was selected on each side. These chords are commonly referred to as strut chordae. One marker was placed on each papillary muscle tip near the origin of the these strut chordae and one each on the anterior leaflet at the point of insertion (markers 30 and 23). After marker placement, miniature strain gauges were sutured to the two strut chordae, with chordal continuity maintained in series with the implanted gauges. Wire snares were secured around the midportion of the chordae above the strain gauge implantation site and exteriorized through the LV wall. Care was exercised to make sure no primary chordae were encompassed by the snare. After completion of the surgical procedure, the animals were weaned from cardiopulmonary bypass, transferred to the experimental catheterization laboratory, and studied intubated with the chest open and under anesthesia with ketamine (1 to 4 mg kg 1 h 1 intravenous infusion) and diazepam (5 mg intravenous bolus as needed). Heart rate control was achieved with an 8 mm IV dose of ULFS49 (Boehringer-Ingelheim, Ridgefield, CT) [13]. Simultaneous biplane videofluoroscopy (60 Hz) and hemodynamic data recordings were obtained over a range of LV filling volumes before and during abrupt preload reduction using vena caval occlusion. Two experimental conditions were studied: (1) baseline and (2) after cutting both second-order anterior chordae. The chordae were severed by passing electrical current through the externalized wire snares. Epicardial color Doppler echocardiography was performed at each time to assess valvular competence and to confirm chordal division. Mitral regurgitation was graded on a 1 to 4 scale (mild, moderate, moderate severe, severe). All animals received humane care in compliance with the Principles of Laboratory Animal Care formulated by the National Society for Medical Research and the Guide for Care and Use of Laboratory Animals prepared by the National Academy of Sciences and published by the National Institutes of Health (DHEW NIHG publication 85-23, revised 1985). This study was approved by the Stanford Medical Center Laboratory Research Animal Review committee and conducted according to Stanford University policy.
3 Ann Thorac Surg TIMEK ET AL 2001;72: ANTERIOR MITRAL LEAFLET SECOND-ORDER CHORDAE 537 Data Acquisition Images were acquired with the animal in the right lateral decubitus position using a Philips Optimus 2000 biplane Lateral ARC 2/Poly DIAGNOST C2 system (Phillips Medical Systems, North America Company, Pleasanton, CA) with the image intensifier in the 9-inch fluoroscopic mode. Data from two radiographic views were digitized and merged to yield 3-D coordinates for each of the radiopaque markers every 16.7 milliseconds using custom-designed software [14, 15]. Aortic pressure, LV pressure, and electrocardiographic voltage signals were digitized and recorded simultaneously during data acquisition. Data Analysis HEMODYNAMIC AND CARDIAC CYCLE TIMING MARKERS. Two consecutive steady-state beats during control and after cutting both second-order AMVL chordae were averaged and defined as the Control and Cut2 data for each animal, respectively. For each cardiac cycle, end-systole was defined as the first videofluoroscopic frame after peak negative LV rate of pressure decrease ( dp/dt), whereas end-diastole was defined as the videofluoroscopic frame containing the peak of the electrocardiographic R-wave. Instantaneous LV volume was calculated every 16.7 milliseconds from the epicardial LV markers using a space-filling multiple tetrahedral volume method [16]. Left ventricular wall mass is included in this calculation of LV volume (therefore, it overestimates LV chamber volume), but this measurement accurately reflects relative changes in LV chamber size. Stroke volume (SV) was the difference between enddiastolic (EDV) and end-systolic (ESV) volume (SV EDV ESV), and ejection fraction (EF) was calculated as (EDV ESV)/EDV. Because systolic LV wall thickening (a major component of SV and EF) cannot be determined using this epicardial marker method, ESV is overestimated, which thereby artifactually lowers our estimates of ejection phase indexes of LV pump performance compared to methods that measure LV chamber (endocardial border) changes; however, relative changes in these calculated measurements are accurate. MITRAL LEAFLET DYNAMICS. Mitral leaflet coaptation at the three locations was defined as the minimum distance measured in 3-D space between opposite leaflet edge markers. To describe the 3-D geometry of the mitral leaflets, marker coordinates were transformed from their original laboratory reference frame to a right-handed Cartesian coordinate system (Fig 1A) with its origin at the midpoint of the line (minor hemiaxis) between the septal and lateral mitral annular markers (markers 14 and 18; Fig 1B). The y-axis is directed from this origin to the LV apex marker, with positive y-axis values indicating positions farther away from the annular plane toward the LV apex. The x-axis is positive toward the lateral (or posterior) LV wall, and the z-axis is orthogonal to the x y plane and is positive toward the posteromedial mitral commissure. To examine leaflet shape under the stresses of systolic pressure, anterior leaflet geometry was determined from the 3-D coordinates of 13 individual anterior leaflet and annular markers 100 milliseconds after enddiastole, at which time LV pressure was near its maximum value. Statistical Analysis All data are reported as mean 1 standard deviation unless otherwise stated. Hemodynamic and markerderived data from two consecutive steady-state beats from each heart were registered in time at end-diastole (t 0). Marker data were analyzed more than 15 frames before and after end-diastole, thus allowing evaluation during a total span of 500 milliseconds. The mean and standard devition for each variable at each sampling instant were computed for 16 beats (2 beats 8 hearts) for Control and Cut2 conditions. Data were compared using two-tailed t test for paired comparisons. Results The weight of the animals was kg; due to the complexity of this experimental preparation, cardiopulmonary bypass time and aortic cross-clamp time were very long ( minutes and minutes, respectively). Postmortem examination revealed that the markers were in proper position and that the largest of the second-order chordae was completely severed. Hemodynamics Hemodynamic data before and after severing secondorder chordae are shown in Table 1. No significant difference in heart rate, LV dp/dt, maximum LV pressure, ejection fraction, EDV, or end-diastolic pressure was present between the two conditions. As previously mentioned, these low ejection fraction values do not represent severe LV systolic dysfunction, but are due to using LV epicardial markers to calculate LV volume, thus not accounting for LV wall thickening during systole and thereby overestimating ESV. Mitral Valve Competence Trace-to-mild mitral regurgitation was detected in all control group animals by color Doppler echocardiography. There was no change in the degree of mitral regurgitation after cutting both second-order chordae (Table 2). Mitral Leaflet Coaptation Mitral leaflet coaptation times during the two conditions are shown in Figure 2 and Table 2. These times did not differ significantly between the two conditions near the anterior commissure, at midleaflet, or near the posterior commissure. Comparing Control and Cut2 conditions, the distance between the anterior papillary muscle tip and the insertion point of its second-order chord on the anterior leaflet (marker 30; Fig 1B) did not change ( cm versus cm at end-diastole and versus cm at end systole [p NS]). Similarly, the distance between the posterior papillary muscle tip and the insertion of the corresponding sec-
4 538 TIMEK ET AL Ann Thorac Surg ANTERIOR MITRAL LEAFLET SECOND-ORDER CHORDAE 2001;72: Table 1. Hemodynamics Control Cut2 p Value HR (min 1 ) NS dp/dt (mm Hg/s) 2, , LVP (mm Hg) EF (%) EDV (ml) NS LVEDP (mm Hg) NS dp/dt maximum positive rate change of LV pressure; EDV LV end-diastolic volume; EF LV ejection fraction; HR heart rate; LVEDP LV end-diastolic pressure; LVP maximum systolic LV pressure; NS not significant. ond-order chord on the anterior leaflet (marker 23; Fig 1B) did not change significantly between Control and Cut2 conditions ( cm versus cm at end-diastole, and cm versus cm at end-systole [p NS]). Mitral Leaflet Shape Systolic 3-D anterior mitral leaflet shape 100 milliseconds after end-diastole is shown in Figure 3. At this time, LV pressure was near its maximum, that is, 97 9mmHg and mm Hg during Control and Cut2, respectively. Statistical analysis of the x, y, and z coordinates of all 13 markers used to determine anterior leaflet shape revealed only a mm lateral displacement of marker 30 with severing of both chordae (p 0.012). All the other markers showed no significant spatial displacement after cutting the second-order chordae. Comment Table 2. Leaflet Coaptation Control Cut2 Leaflet coaptation (msec) ACOM MID PCOM Mitral regurgitation ACOM near anterior commissure; PCOM near posterior commissure. p not significant. MID midleaflet edges; Fig 2. Leaflet edge distance (in centimeters) at midleaflet edge (MID, markers 27 and 28), near the anterior commissure (ACOM, markers 31 and 32), and near the posterior commissure (PCOM, markers 24 and 25) during control (solid squares) and after cutting both second-order chordae (open circles). A 500-millisecond time window centered at end-diastole (t 0) is shown for both conditions. Error bars indicate one standard error of the mean. The importance of the mitral subvalvular apparatus in performing its dual role optimizing LV systolic function and assuring valvular competence is well established [9, 10]. Although described anatomically almost a century ago [17], the precise role of second-order chordae tendineae has not yet been clearly defined. As the indications for mitral valve repair expanded with the introduction of innovative surgical repair techniques, surgical reconstruction using second-order chordae entered the clinical arena [6, 7, 18, 19]. This is distinctly different from the old practice of resecting or debulking or fenestration of thickened and scarred second-order chordae in patients with rheumatic mitral pathology [5, 20]. Currently, second-order chordal transposition is helpful for correcting anterior leaflet prolapse, but the effects of moving second-order chordae to the leading edge of the leaflet on valvular geometry and function have not been investigated previously either in vivo or ex vivo. This study was designed to investigate the effect of severing anterior second-order chordae on valve competence and leaflet geometry in sheep. We observed that neither valve competence, leaflet edge separation, nor leaflet geometry was altered by cutting the anterior second-order chordae. Leaflet coaptation was unchanged near the anterior commissure, at the midleaflet edge, nor near the posterior commissure after transection of both second-order chordae. No significant mitral regurgitation was noted. This provides evidence that the two large (or strut ) anterior second-order chordae do not play a crucial role in maintaining normal leaflet coaptation and valvular competence, at least in normal sheep hearts. Recent experiments exploring the differential functional roles of first-order and second-order chordae in an isolated working pig heart model support this conclusion [11]. In that experiment, good leaflet coaptation and no mitral regurgitation occurred after cutting the anterior secondorder chordae. Although no hemodynamic differences
5 Ann Thorac Surg TIMEK ET AL 2001;72: ANTERIOR MITRAL LEAFLET SECOND-ORDER CHORDAE 539 Fig 3. Three-dimensional representation of anterior mitral leaflet geometry 100 milliseconds after end-diastole during control (solid squares) and after cutting both second-order chordae (open circles). Marker numbers correspond with those labeled in Figure 1B. (ACOM anterior commissure; PCOM posterior commissure.) were observed after chordal severance in our study, the isolated heart data revealed a decrease in LV pump function (as assessed by load-dependent measures) after dividing the anterior second-order chordae. This apparent discordance may be due to the number of chordae cut, species differences, in vivo versus ex vivo experimental models, hemodynamic condition of the heart under study (our animals has just undergone a prolonged procedure on cardiopulmonary bypass), or a combination of these factors. As illustrated in Figure 3, 3-D leaflet geometry was maintained after chordal severing, and no gross alterations in leaflet shape were apparent apart from the small lateral displacement of one leaflet marker. During the period when LV pressure was reaching its maximum (100 milliseconds after end-diastole), the anterior leaflet retained a compound shape in both experimental conditions, being partially concave to the LV cavity as reported previously [21]. No leaflet prolapse or billowing was evident, and the line of coaptation remained on the LV side of the plane of the mitral annulus. It should be noted, however, that we divided only one of several secondary chordae in this experiment. In vitro studies using stress-strain analysis on excised porcine mitral chordae by Kunzelman and Cochran [22] have shown first-order chordae to be much stiffer than second-order chordae and that the stress on the first-order chordae was higher than on the second-order chordae at any given degree of strain. Therefore, these investigators postulated that due to their number and mechanical properties, first-order (previously termed marginal or primary) chordae bear the bulk of systolic pressure load exerted on the mitral leaflets. This implied that removal of some of the second-order (also called basal) chordae may not greatly affect chordal stress distribution. These experiments corroborate our findings as only a slight change in leaflet shape was seen immediately after cutting the second-order chordae. Preserved leaflet geometry after second-order chordae severing suggests that there is considerable chordal redundancy and stress redistribution reserve that prevents leaflet deformation in the absence of intact second-order chordae. We also found that the distance between the chord papillary tip origin and leaflet insertion site was unchanged both at enddiastole and end-systole after chordal severing. Thus, no leaflet billowing occurred at these insertion sites, further supporting the notion that second-order chordae do not play a cardinal role in maintaining normal leaflet geometry and coaptation under these experimental conditions. The absence of perturbed leaflet geometry after secondorder chordae transection in this experiment, however, does not exclude abnormal stress distribution on the first-order chordae, which could lead to altered leaflet shape or mitral insufficiency over the long term. Furthermore, other in vitro experiments using excised porcine valves suggest that second-order chordae may mediate leaflet tethering in the setting of apical displacement of papillary muscles, as might be seen in patients with ischemic mitral regurgitation [23]. Although one must always be cautious in extrapolating the results of open-chest animal experiments to the closed-chest human situation, these data confirm that second-order chordae are not key to maintaining valve competence in human hearts. Although no acute change in geometry was observed under admittedly low systolic pressure in the study, no comment can be made on the possible long-term consequences on leaflet geometry and shape after dividing the second-order chordae tendineae. We did not study chordal transposition in this experiment, but our data suggest that the use of these chords in mitral valve repair may not be deleterious to anterior leaflet dynamics. Future studies are needed to investigate the chronic effects of second-order strut chordae transection on valve geometry, shape, and function. Study Limitations The above results must be interpreted in light of several limitations inherent in this experiment. Implanting the strain gauges in the second-order chordae may have altered normal chord tension, but these chordae were never slack as continuous positive tension was recorded before transection. The data were obtained in an acute, open-chest setting immediately after a long and complicated cardiac procedure, which is far removed from normal clinical circumstances. Thus, no direct implications can be made regarding the long-term effects of second-order chordal transection on valvular leaflet function. It is plausible that severing of the chordae resulted in maldistribution of stresses on the remaining chordae, which could ultimately become manifest as perturbed leaflet geometry or valvular insufficiency over time. This possibility cannot be excluded based on our
6 540 TIMEK ET AL Ann Thorac Surg ANTERIOR MITRAL LEAFLET SECOND-ORDER CHORDAE 2001;72: data due to the acute nature of this experiment. Clinical observations, however, do not seem to support this possibility and experimental findings suggest that the first-order chordae carry the bulk of systolic stress under normal leaflet loading conditions. Furthermore, we did not study chordal transposition per se but only the effect of second-order chord transection on anterior leaflet kinematics and how it may relate to mitral valve repair. Although these limitations limit the clinical applicability of these data, this experiment sheds some light on the physiologic function of mitral second-order chordae. In addition, these experiments were performed in normal animal hearts without the associated pathophysiologic changes that often accompany chronic mitral regurgitation in patients. Differences in comparative anatomy between human and sheep mitral valves must also be considered, as the observed results may not directly apply to the human mitral valve. Our determination of leaflet geometry and time of coaptation used nine small metal markers sutured to the anterior mitral leaflet, which could have altered normal leaflet motion. This is unlikely as experiments in this laboratory in sheep with large overload of the anterior leaflet with increasing numbers of excessively large markers (up to approximately four times the aggregate mass of the current markers) revealed no change in peak opening velocity and peak E-wave velocity compared to a leaflet without markers when assessed with epicardial pulse wave and continuous wave Doppler echo. It must also be mentioned that this experiment consisted of a small number of animals (n 8); although the paired design of the experiment provides confidence to the statistical conclusions, the chance that a or type II statistical error is present cannot be ignored. We appreciate the superb technical assistance provided by Mary K. Zasio, BA, Carol W. Mead, BA, and Erin M. Schultz, BS. This work was supported in part by grants HL and HL from the National Heart Lung, and Blood Institute. Doctors Timek, Green, and Dagum are Carl and Leah McConnell Cardiovascular Surgical Research Fellows. Doctor Timek is also a recipient of the Thoracic Surgery Foundation Research Fellowship Award and NHLBI Individual Research Service Award HL Doctors Green and Dagum were also supported by NHLBI Individual Research Service Awards HL and HL10000, respectively. Doctors Nielsen and Hasenkam were supported by grants from The Danish Heart Foundation, The Danish Medical Research Council, and The Research Initiative of Aarhus University Hospital. References 1. Deloche A, Jebara VA, Relland, et al. Valve repair with Carpentier techniques. J Thorac Cardiovasc Surg 1990;99: Reul RM, Cohn LH. Mitral valve reconstruction for mitral insufficiency. Prog Cardiovasc Dis 1997;39: Dreyfus G, Al Ayle N, Dubois D, de Lentdecker P. Long term results of mitral repair: posterior papillary muscle repositioning versus chordal shortening. Eur J Cardiothorac Surg 1999;16: Maisano F, Torracca L, Oppizzi M, et al. The edge-to-edge technique: a simplified method to correct mitral insufficiency. Eur J Cardiothorac Surg 1998;13: Carpentier A. Cardiac valve surgery: the French correction. J Thorac Cardiovasc Surg 1983;86: Uva MS, Grare P, Jebara V, et al. Transposition of chordae in mitral valve repair. Circulation 1993;88: Grossi EA, Galloway AC, LeBoutillier M, et al. Anterior leaflet procedures during mitral valve repair do not adversely influence long-term outcome. J Am Coll Cardiol 1995;25: Smedira NG, Selman R, Cosgrove DM, et al. Repair of anterior leaflet prolapse: chordal transfer is superior to chordal shortening. J Thorac Cardiovasc Surg 1996;112: Sarris GE, Fann JI, Niczyporuk MA, Derby GC, Handen CE, Miller DC. Global and regional left ventricular systolic performance in the in situ ejecting canine heart: importance of the mitral apparatus. Circulation 1989;80(Suppl 1):I David TE, Burns RJ, Bacchus CM, Druck MN. Mitral valve replacement for mitral regurgitation with and without preservation of chordae tendinae. J Thorac Cardiovasc Surg 1984; 88: Obadia JF, Casali C, Chassignolle JF, Janier M. Mitral subvalvular apparatus: different functions of primary and secondary chordae. Circulation 1997;96: Glasson JR, Komeda M, Daughters GT, et al. Most ovine mitral annular three-dimensional size reduction occurs before ventricular systole and is abolished with ventricular pacing. Circulation 1997;96(Suppl 2):II Schipke JD, Harasawa Y, Suigura S, Alexander J, Burkhoff D. Effect of a bradycardic agent on the isolated blood-perfused canine heart. Cardiovasc Drugs Ther 1991;5: Niczyporuk MA, Miller DC. Automatic tracking and digitization of multiple radiopaque myocardial markers. Comput Biomed Res 1991;24: Daughters GT, Sanders WJ, Miller DC, Schwarzkopf A, Mead CW, Ingels NB. A comparison of two analytical systems for 3-D reconstruction for biplane videoradiograms. Comp in Cardiol 1988;15: Moon MR, DeAnda A, Daughters GT, Ingels NB, Miller DC. Experimental evaluation of different chordal preservation methods during mitral valve replacement. Ann Thorac Surg 1994;58: Tandler J. Anatomie des Herzens. Jena, Germany. Gustav Fischer Verlag, 1913: Bernal JM, Rabasa JM, Olalla JJ, Carrion MF, Alonso A, Revuelta JM. Repair of chordae tendinae for rheumatic mitral valve disease: a twenty-year experience. J Thorac Cardiovasc Surg 1996;111: Salati M, Scrofani R, Fundro P, Cialfi A, Santoli C. Correction of anterior mitral prolapse: result of chordal transposition. J Thorac Cardiovasc Surg 1992;104: Antunes MJ, Magalhaes MP, Colsen PR, Kinsley RH. Valvuloplasty for rheumatic mitral valve disease: a surgical challenge. J Thorac Cardiovasc Surg 1997;94: Karlsson MA, Glasson JR, Bolger AF, et al. Mitral valve opening in the ovine heart. Am J Physiol 1998;274:H Kunzelman KS, Cochran RP. Mechanical properties of basal and marginal mitral valve chordae tendinae. Trans ASAIO 1990;36:M He S, Weston MW, Lemmon J, Jensen M, Levine RA, Yoganathan AP. Geometric distribution of chordae tendineae: an important anatomic feature in mitral valve function. J Heart Valve Dis 200;9:
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