Mechanism of Function of the Mitral Valve Leaflets, Chordae Tendineae and Left Ventricular Papillary Muscles in Dogs

Transcription

1 Mechanism of Function of the Mitral Valve Leaflets, Chordae Tendineae and Left Ventricular Papillary Muscles in Dogs By Stephen Karas, Jr., M.D., and Ronald C. Elkins, M.D. ABSTRACT In five dogs (18 to 28 kg) under pentobarbital anesthesia metal clips were placed on the free margin of the anterior and posterior mitral valve leaflets, and on the epicardial surface of the left ventricle at the apex and at the base. After full recovery cineangiograms were taken in the right anterior oblique and right lateral position and the length from the apex of the left ventricle to the free margins of the mitral valve leaflet was measured. The average distance between the apex and the free margin of the anterior leaflet in two dogs and on a clip placed on the chordae tendineae above the anterior leaflet in two dogs was the same during slow ventricular, atrial systole, and during ventricular ejection. The average distance between the apex and the free margin of the posterior leaflet in three dogs was also the same during the same time periods in the cardiac cycle. The maintenance of the same distance between the free margin of the mitral valve leaflet and the apex during diastole when the papillary muscle is relaxed and during systole when it is contracted suggests that the papillary muscle contracts isometrically. ADDITIONAL KEY WORDS heart valves isometric contraction rapid ventricular slow ventricular atrial systole isovolumetric systole ventricular ejection This work describes the results of experiments designed to find out whether the distance from the apex of the heart to the free margin of the mitral valve stays the same throughout the cardiac cycle or, in other words, whether the papillary muscle contracts isometrically. The mitral valve opens during diastole, allows blood to enter the ventricle, and closes at the end of systole to prevent retrograde flow. Very exact timing and extent of valve opening and closing are necessary to insure proper valve function. Mitral valve motion has been extensively studied with cineangiograms by Rushmer (1) and more recently with ultrasound (2-4). The ultrasound From the Departments of Physiology and Surgery, The Johns Hopkins University School of Medicine, Baltimore, Maryland This work was supported in part by the U. S. Public Health Service Grant 5 TO1 GMO1541 from the National Institutes of Health. Dr. Elkins is a trainee in academic surgery. Received May 26, Accepted for publication April 13, studies have shown that the valve opens widest during rapid- diastole, partially closes during slow- diastole, opens wide with atrial systole, and closes completely during systole. The mitral leaflet attach at their bases to the left ventricle and at their margins to the chordae tendineae, which in turn are connected to the papillary muscles, so that changes in ventricular shape probably also influence valve motion. The curve for the motion of the mitral valve measured in human beings using ultrasound (5) and the changes in left ventricular apexto-base length measured by mercury strain gauges in dogs (6) appear to be parallel. Shortening of the distance from the apex to the base of the left ventricle in early systole is proportional to the retrograde movement of the mitral leaflets, and during diastole with a lengthening of the apex-to-base length there is a proportional downward motion of the leaflet. Such a parallel motion of the free margin of the valve with changing apex-tobase length can be explained if the distance 689

2 690 KARAS, ELKINS FIGURE 1 Right: Stainless steel spring-loaded clips. Left: Clip in holder used for insertion. from the apex to the free margin does not change throughout the entire cardiac cycle. Methods In five anesthetized dogs (pentobarbital, 20mg/kg) a left lateral thoracotomy was performed under sterile conditions. A purse-string suture was placed at the apex of the left ventricle and in the left atrial appendage. Through a stab wound in the apex of the left ventricle the clip holder with attached clip (Fig. 1) was advanced into the left ventricular cavity. Using a finger through the left atrial appendage into the left atrium as a guide, the metal spring-loaded clips, weighing 130 mg, were placed on the free margins of the anterior and posterior leaflets of the mitral valve in three dogs (Fig. 2, left), and in two dogs a clip was placed on a chorda tendineae above the anterior papillary muscle and on the free margin of the posterior leaflet of the mitral valve. After placement of the clips, the clip holder was removed and the purse strings were tied for hemostasis. This technique is similar to the approach used for transventricular mitral commissurotomy. Additional small metal nerve clips were sewn on the epicardium of the left ventricle at the apex and on the anterior and posterior aspect of the base (Fig. 2, right). The pericardium was closed loosely, the chest closed and the dogs were allowed to recover from the operation for a week or more. Three dogs were reanesthetized after recuperation. Cineangiograms were taken at 30 and 60 frames/ sec in the right lateral, right anterior oblique, left lateral, and left anterior oblique positions. The electrocardiogram and phonocardiogram were recorded and simultaneous left ventricular and atrial pressures, and radiopaque dye injections were performed. Two dogs (dogs 4 and 5) were trained to lie Apex- ft»tpap.tn FIGURE 2 Left: Location of nerve clips 2 and 3 on anterior and posterior aspect of the base and clip 1 at apex in dog 1. Right: With opened left ventricular chamber of same heart showing clips placed on the margin of the anterior and posterior leaflet of the mitral valve.

3 MECHANISM OF MITRAL VALVE FUNCTION 691 quietly on their right side so that cineangiograms in the right lateral position could be obtained without anesthesia. These dogs were then anesthetized and simultaneous left ventricular and left atrial pressures were obtained. In dog 1, 50 consecutive heart beats were analyzed. The distances measured in this dog were: (1) between the clip on the anterior leaflet and clip 1 at the apex, and (2) between clip 2 at the base and clip 1 at the apex. In dog 2, 24 consecutive heart beats were analyzed and the distances measured were between the free margin of the posterior leaflet and the apex (clip 1). In dog 3, 14 consecutive heart beats were analyzed and the distance between a clip placed on a chorda tendineae 2 mm above the anterior papillary muscle and the apex (clip 1) was measured. In dog 4, 15 consecutive heart beats were analyzed and the distances measured were: (1) between a clip on the anterior leaflet and clip 1 at the apex, and (2) between a clip on the posterior leaflet and clip 1 at the apex. In dog 5, 14 consecutive heart beats were analyzed and the distance between a clip placed on the chordae tendineae 10 mm above the anterior papillary muscle and the apex (clip 1) and the distance between a clip on the posterior leaflet and the apex (clip 1) were measured. Measurements of mitral valve motion were made in the right anterior oblique and right lateral position because in these positions the anterior leaflet is viewed perpendicular to its major axis of motion. Such a position permitted viewing of the maximum amount of clip motion (3). Simultaneous left atrial and left ventricular pressure measurements demonstrated no gradient across the valve in diastole and left ventricular radiopaque medium injections revealed no mitral regurgitation, indicating normal physiologic function of the mitral valve with the clips in place. TABLE 1 Average Distance between Spring-Loaded Clip and Apex Clip Dog no No. of beats Spring-loaded clip position Free margin of anterior leaflet Free margin of posterior leaflet On chordae tendineae 2 mm above anterior papillary muscle Free margin of anterior leaflet On chordae tendineae 10 mm above anterior papillary muscle Free margin of posterior leaflet Rapid ventricular 40.0 mm (SD ±.97 mm) 48.0 mm (SD ±.27 mm) 37.8 mm (SD ±.19 mm) 41.0 mm (SD ±.78 mm) 46.7 mm (SD ±.78 mm) 56.2 mm (SD ± 1.35 mm) The cineangiograms were viewed in four positions (right lateral, right anterior oblique, left lateral, left anterior oblique) in three of the animals and measurements were made in two positions (right anterior oblique and right lateral) in an effort to rule out measurement errors due to rotary motion of the heart and altered x-ray tube to clip distances. There were no easily detectable differences in the movements of the clips and no correction for the altered x-ray tube to clip distance was felt necessary. Also the absolute length of the clip (7.5 mm) was observed throughout the cardiac cycle and no significant change in length was noted in the four positions. The measurements of the distance between the clips on the free margins of valve leaflet and the apex includes alterations in the absolute thickness of the ventricular wall at the apex as well as alterations in the papillary muscle length. Possible errors in measurement due to changes in the thickness of the ventricular wall were felt to be so small that they could be disregarded. The animals were killed after obtaining the cineangiograms and pressure measurements. The relationships of the clips on the free margin of the mitral valve and chorda tendineae to the apex clip were verified. In each case a line drawn between the clips on the valve leaflet and the apex were nearly parallel to a line drawn from the midpoint of the valve leaflet through the mid-longitudinal portion of the papillary muscle. Results In five dogs studied, the average distance between the tip of the spring-loaded clip and the apex is shown in Table 1. In the two unanesthetized dogs the measurements were Slow ventricular & atrial systole 42.4 mm (SD ±.20 mm) 48.0 mm (SD ±.27 mm) 37.8 mm (SD ±.19 mm) 41.5 mm (SD ±.09 mm) 47.5 mm (SD ±.05 mm) 60.0 mm (SD ±.16 mm) Isovolumetric systole 43.4 mm (SD ±.85 mm) 48.0 mm (SD ±.27 mm) 40.0 mm (SD ±.56 mm) 42.8 mm (SD ±.55 mm) 48.8 mm (SD ± 1.15 mm) 61.2 mm (SD ±.70 mm) Ventricular ejection 42.2 mm (SD ±.16 mm) 48.0 mm (SD ±.27 mm) 37.8 mm (SD ±.19 mm) 41.5 mm (SD ±.13 mm) 47.5 mm (SD ±,14 mm) 60.0 mm (SD ±.05 mm)

4 692 KARAS, ELKINS more widely scattered (note larger standard deviations) due to the normal sinus arrhythmia that occurred in these dogs. A typical beat recorded from dog 1 shows the changes in distance between the free margin of the anterior leaflet and the apex (Fig. 3, top). During rapid ventricular this distance shortens to 39 mm, then returns to 42 mm during slow ventricular s and atrial systole. With isovolumetric systole this distance lengthens to 44 mm to return during ventricular ejection to 42 mm, the same length as it was during slow ventricular and atrial systole. The range of the motion of the anterior leaflet clip in the same beat was about 12 mm from the farthest anterior (open) to the farthest posterior (closed) position. At the beginning of rapid ventricular the anterior leaflet moved rapidly anterior to its farthest open position, closed half way during slow ventricular, opened again with atrial systole and closed to farthest posterior position during isovolumetric systole (Fig. 3, middle). In contrast, the posterior leaflet moved only 7 mm from its farthest anterior to its farthest posterior position. Comparison of motion of the posterior leaflet clip with that of the ventricular wall just behind it as outlined by dye injection showed that the posterior leaflet motion was identical to the ventricular wall motion. During ventricular the posterior leaflet and the wall both moved posteriorly and during ventricular ejection both moved anteriorly. Apex-to-base length increased during diastole and decreased during systole (Fig. 3, bottom). Discussion and Conclusion The maintenance of a constant distance between the free margin of the valve leaflet and the apex during slow ventricular and atrial systole when the papillary muscle is relaxed and during ventricular ejection when it is contracted supports the hypothesis that the papillary muscle contracts isometrically. This is confirmed by the constant distance 40 Slow Ventriculo Filling ond Atral Systole ANTERIOR ond POSTERIOR CLIP MOTION I TIME(.O33 sec/frame) FIGURE 3 Measurement of clip motion in dog 1 from cineangiogram, examples of which are shown in Figure 5. Top: Distance between apex to tip of anterior leaflet showing maintenance of the same apex to free margin (tip length) length through most of diastole and most of systole with the exception of rapid ventricular and isovolumetric systole (see text for explanation). Middle: Motion of anterior and posterior leaflet clip showing relatively larger excursion of anterior leaflet clip motion compared to posterior leaflet clip motion. Bottom: Motion of base upward during diastole and downward during systole. Circulation Research. Vol. XXVI, June 1970

5 MECHANISM OF MITRAL VALVE FUNCTION 693 found between clips on the chorda tendineae and the apex. This critical distance between the free margin of the valve and the apex is kept constant by the chordae tendineae and the papillary muscle so that the valve can open and close appropriately. If the papillary muscle shortened during ventricular contraction it would prevent apposition of the leaflets, hence allow regurgitation. A more thorough description of mitral valve function is necessary to explain the changes found consistently in the distance between the free margin of the valve and apex during rapid ventricular and during isovol- A. Rapid ventricular C. Atrial systole D. Slow ventricular '1 i D. Isovol u metric systole E. Ventricular eject ion FIGURE 4 Cineangiogram taken at 60 frames/sec of dog 1 in right anterior oblique (RAO) position showing catheter in aorta. Nerve clips at apex (1) and on anterior and posterior (2 and 3) aspects of the base dividing left ventricle (LV) and atrium (AT). The spring-loaded clips are located on the free margins of the anterior leaflet (AL) and posterior leaflet (PL). The position of the clips showing at five stages of the heart cycle rapid ventricular, slow ventricular, atrial systole, isovolumetric systole, and ventricular ejection. The distance between tip of anterior leaflet to apex (AL to clip 1) is identical during both slow ventricular and atrial systole and ventricular ejection.

6 694 KARAS, ELKINS umetric systole (Fig. 3, top). These distance changes can best be understood if the interrelationship of the motion of the anterior and posterior leaflet with the moving walls of the ventricle is considered throughout the cardiac cycle. Significant mitral valve motion occurs during five periods of the cardiac cycle: (1) rapid ventricular, (2) slow ventricular, (3) atrial systole, (4) isovolumetric systole (aortic valve closed), and (5) ventricular ejection (aortic valve opened). Isovolumetric relaxation is not included as mitral valve motion is minimal during this period. Rapid Ventricular Filling. At the time of rapid ventricular as the heart muscle relaxes from its contracted position in late systole (Fig. 5A), ventricular pressure falls, left atrial pressure exceeds left ventricular pressure, and blood rushes rapidly from the atrium to the ventricle, forcing open the anterior leaflet to its farthest extent. At this time the chordae tendineae and papillary muscle are slack because the distance between A. Rapid ventricular B. Slow ventricular C. Atrial systole D. Isovolumetric systole E. Ventricular ejection FIGURE S Mitral valve, chordae tendineae, and papillary muscle function during the same five stages of the cardiac cycle illustrated in Figure 4 (see text for explanation). Circulation Research. Vol. XXVI. June 1970

7 MECHANISM OF MITRAL VALVE FUNCTION 695 the free margin of the valve and the apex is much shorter than at any other time in the cardiac cycle (Fig. 3, top). The valve leaflet opens into a small relaxed ventricle and is allowed freedom of motion. During rapid ventricular the ventricular chamber enlarges as the base moves up and the sides out, (throughout the entire cardiac cycle the apex motion is minimal). This ventricular expansion appears to make the papillary muscle and chordae tendineae tense, because the length between the free margin of the valve and the bottom of the ventricle returns to the constant longer length maintained throughout the rest of the cardiac cycle (Figs. 4Aand5A). Slow Ventricular Filling. During slow ventricular or diastasis the valve leaflets remain at a position midway between fully opened and closed (Figs. 4B and 5B). Atrjal systole. When the atrium contracts, blood is forced into the expanded ventricle forcing the valve leaflet open in the ventricle (Figs. 4C and 5C). Now with the chordae tendineae and papillary muscle tensed the valve is allowed less freedom and does not open as far as it did during rapid ventricular. As the atrium relaxes, the valve returns to its equilibrium position once again. Isovolumetric systole. The force of ventricular contraction is so great and ventricular dimensions change so rapidly that the valve leaflets are closed abruptly and the distance between the free margin of the valve and the apex is a little longer than at any other time in the cycle (Fig. 3, top). This observation is supported by those of Cronin (6) and of F. Kavaler (personal communication) who noted initial lengthening of the left ventricular papillary muscle during isovolumetric systole (Figs. 4D and 5D), and Cronin felt that this lengthening was probably the result of a delay in papillary muscle contraction as left ventricular pressure was observed to rise considerably in advance of the development of increased tension in the papillary muscle. The closing of the anterior leaflet during isovolumetric systole is much like the fitting of a key into the keyhole provided by the posterior leaflet. The posterior or mural leaflet, smaller in length but larger in circumference than the anterior leaflet, is the surface upon which the anterior leaflet can close. In fact it acts very much as its name "mural" suggests and its motion is identical with that of the ventricular wall behind it. Ventricular Ejection with Aortic Valve Open. As soon as the aortic valve opens, the contracting ventricle forces the blood into the aorta (Figs. 4C and 5C). The base moves down and the sides in as the blood is emptied from the ventricle. During this time, the free margin of the valve stays the same distance from the apex as it did during diastole due to the movement of the valve toward the left atrium. This maintenance of a constant distance indicates that contraction of the papillary muscle during systole must be isometric. In summary, there are three periods during the normal cardiac cycle when the distance between the apex of the left ventricle and free margin of the mitral valve is altered. The first is a shortening of this distance when the mitral valve opens and rapid ventricular occurs. The second is a resumption of the length found throughout the remainder of diastole and ventricular ejection. The third is an increased distance found during isovolumetric systole which is probably due to a delay in the contraction of the papillary muscles. The maintenance of a constant distance between the free margin of the leaflet and the apex during slow ventricular and atrial systole when the papillary muscle is relaxed and during ventricular ejection when it is contracted supports the hypotheses that the papillary muscle contracts isometrically. This isometric contraction of the papillary muscle appears to be important to mitral valve function so that proper apposition of the leaflets can occur and a competent atrioventricular valve can be maintained during the rapid pressure and ventricular volume changes of the normal heart beat. Acknowledgment We wish to express our thanks to Dr. William Milnor for encouragement and suggestions, Dr.

8 696 KARAS, ELKINS Gottlieb Friesinger for advice, Dr. William C. Roberts for reviewing the manuscript, Mr. Fred Jackson for 4. operating assistance, Mr. Al Austin for catheterization help and Miss Lynn McDowell for the drawings. References ~ 1. RuSHMEH, R. F., FlNLAYSON, B. L., AND NASH, A. A.: Movement of the mitral valve. Circ Res 4: 337, HERTZ, H. C: Ultrasonic engineering in heart diagnosis. Amer J Cardiol 19: 18, SEGAL, B. L.: Echocardiography-ultrasound car- diography. Amer J Cardiol 19: 1, ZAKY, A., GBABHORN, L., AND FEIGENBAUM, H.: Movement of the mitral ring: A study in ultrasoundcardiography. Cardiovasc Surg 1: 121, DAYEM, A., GRABHOBN, L., AND FEICENBAUM, H.: Movements of the mitral valve annulus. Cardiovas Res 1: 116, CRONIN, R., ARMOUR, J. A., AND RANDALL, W. C.: Function of the in-situ papillary muscle in the canine left ventricle. Cardiovas Res 25: 67, 1969.