Papillary Muscle Perfusion Pattern
A Hypothesis for Ischemic Papillary Muscle Dysfunction
Background The pathogenesis of posterior papillary muscle dysfunction is poorly understood. We hypothesized that papillary muscle perfusion pattern may explain the higher prevalence of posterior papillary muscle dysfunction after myocardial infarction.
Methods and Results Twenty patients were monitored by transesophageal echocardiography during coronary surgery. Superselective coronary graft injections of 0.2 to 0.5 mL of sonicated albumin microbubbles were performed to assess graft patency and papillary muscle perfusion. Thirty-five graft injections were analyzed: 13 in the right coronary artery, 15 in an obtuse marginal branch, 1 in the left anterior descending coronary artery, and 6 in the first diagonal branch. The posterior papillary muscle was opacified in 16 patients, 11 from the right coronary artery and 5 from one obtuse marginal branch. In 10 of 16 patients (63%), the papillary muscle was perfused by one vessel, while in 6 of 16 (37%), it was perfused by two vessels. The anterior papillary muscle was opacified in 14 patients. Ten patients (71%) had double-vessel and 4 (29%) had single-vessel supply. In the subgroup of 10 patients with old inferior myocardial infarction, mitral regurgitation was present only among those 6 with single rather than double blood supply (P<.05).
Conclusions Myocardial infarction may cause papillary muscle dysfunction when the blood supply is provided by one rather than two vessels, as is more frequently the case with the posterior rather than the anterior papillary muscle.
Papillary muscle dysfunction or rupture is a rare but catastrophic consequence of acute myocardial infarction; the posterior papillary muscle is involved in about 75% of cases and the anterior in about 25%. However, despite extensive anatomic and clinical studies on papillary muscle vasculature since 1885,1 the reason for this difference has still not been determined.2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
Myocardial contrast echocardiography has recently been introduced to study the intramyocardial distribution of coronary blood flow.18 19 20 21 22 This technique has been used during cardiac surgery to monitor cardioplegia distribution23 24 25 and to assess coronary artery graft patency and the area at risk of graft occlusion.26 27 28
The aim of this study was to investigate by myocardial contrast echocardiography the perfusion pattern of papillary muscles in patients undergoing coronary artery bypass graft surgery and thus to test whether a difference in regional blood flow distribution may explain the higher prevalence of posterior papillary muscle disease in patients with old inferior myocardial infarction.
Twenty patients 37 to 70 years old undergoing coronary artery bypass graft surgery for symptomatic coronary artery disease were enrolled in this study. All patients had stable angina pectoris. Twelve patients had had previous myocardial infarction: inferior in 10, anterolateral in 1, and anteroseptal in 1. The protocol was approved by the institution’s Ethics Committee, and informed consent was obtained from all patients. Exclusion criteria included poor left ventricular function with ejection fraction <30% as assessed by cineventriculography, severe mitral regurgitation (grade 3 to 4 by angiography), mitral valve prolapse, concomitant valvular heart disease, severe left ventricular hypertrophy, diabetes mellitus, and renal disease with creatinine level >2 mg/dL.
All 20 patients underwent preoperative coronary angiography in multiple projections; 17 had three-vessel and 3 had two-vessel coronary artery disease. Coronary artery dominance was assigned to the artery supplying the posterior descending coronary artery. According to these criteria, all patients had right coronary artery dominance.
Contrast Agent Preparation
The echocontrast agent was prepared under sterile conditions 1 hour before surgery following a standardized protocol,29 30 31 according to which 8 mL of 5% human albumin is exposed to 125 W of ultrasound energy until the albumin denaturation point is reached. At 10-second intervals, air is added to the solution to improve cavitation. At the end of the procedure, the solution separates into two layers: an upper, opaque white layer containing an excess of large and nonuniform bubbles and a lower, opalescent gray layer containing a suspension of 4±1-μm microbubbles. The contrast agent is then stored in 1-mL insulin syringes at room temperature. Albumin microbubbles thus produced have an in vitro half-life of at least 6 months. They are nontoxic, do not impede flow through the capillaries,32 and do not alter systemic blood flow.33
Anesthesia was induced with fentanyl 30 to 35 μg/kg, diazepam 0.25 to 0.5 mg/kg, and succinylcholine 1.5 mg/kg and maintained with fentanyl, droperidol, pancuronium bromide, and a 50% nitrous oxide/50% oxygen mixture. The tip of a Swan-Ganz catheter was introduced percutaneously into the pulmonary artery via the internal jugular vein. The radial artery was catheterized to monitor arterial blood pressure. ECG monitoring was performed by means of three peripheral leads.
Patients were monitored by single-plane transesophageal echocardiography. Mitral valve competence was assessed by scanning the mitral valve from the anterior to the posterior mitral commissure. The probe was then advanced to the gastric fundus at a distance of 40 to 45 cm from the incisors and flexed anteriorly to obtain a left ventricular short-axis view at mid–papillary muscle level. This projection includes the distribution territories of the three main coronary vessels and their major branches. Echocardiographic images were recorded before, during, and after contrast injection. No cardiac pacing was used before or after surgery.
Coronary artery bypass graft surgery was carried out with systemic hypothermia (25°C to 28°C) during cardiopulmonary bypass. Myocardial protection was achieved by topical hypothermia (iced saline slush), and cold (4°C) potassium crystalloid cardioplegia solution was administered in the cross-clamped aortic root every 20 to 30 minutes throughout the ischemic period. Left ventricular venting was performed through the aortic root.
A total of 68 grafts (3.4 grafts per patient) were sutured. Forty-nine consisted of inverted saphenous vein and 19 of internal mammary artery. Distal saphenous vein anastomosis was sutured first, and additional cardioplegia was instilled through the proximal free end of the graft. Proximal anastomosis was performed with partial aortic occlusion and during the rewarming phase of cardiopulmonary bypass.
The echocontrast agent was injected in a 0.2- to 0.5-mL bolus with a 25-gauge insulin needle in the vein graft after separation from cardiopulmonary bypass and with the patient in stable hemodynamic condition. The 0.2-mL doses were injected into the smallest vessels, usually the right coronary artery and obtuse marginal branches of the circumflex, and the 0.5-mL doses were injected into the largest vessels, the left anterior descending and first diagonal branch. Thirty-five vein grafts were studied with 43 injections; 8 injections resulted in ultrasound attenuation, and the injection was repeated at a smaller volume. A total of 35 injections were thus analyzed: 13 in the right coronary artery, 15 in an obtuse marginal branch of the circumflex artery, 1 in the left anterior descending artery, and 6 in its first diagonal branch.
Regional Myocardial Perfusion Analysis
Two experienced observers evaluated myocardial opacification by magnetic tape review. Segmental opacification was related to the injected vessel. Percent myocardial opacification was calculated by planimetric measurements of the reperfused area in relation to total left ventricular area.
Papillary Muscle Perfusion
Papillary muscle blood supply was considered single when graft injection resulted in complete opacification of the muscle and double when graft injection produced only partial papillary muscle opacification.
Assessment of Safety
To detect whether changes in regional systolic function occurred during contrast injection, percent systolic wall thickening (PSWT) of the opacified myocardial segments was measured. Myocardial wall thickness was measured in the median portion of each segment in end systole (SWT), corresponding to the smallest left ventricular cavity area, and in end diastole (DWT), corresponding to the spike of the ECG R wave. PSWT was measured before contrast injection and during myocardial opacification according to the formula PSWT=(SWT−DWT)/DWT×100.
Statistical analysis was performed by the Fisher exact probability test to examine the influence of previous inferior myocardial infarction on the onset of mitral regurgitation in patients with single versus double arterial supply to the posterior papillary muscle. A value of P≤.05 was considered significant.
Myocardial Distribution of the Grafts
Papillary muscle perfusion was obtained in 30 of 35 graft injections. The opacified myocardial segment corresponded to the injected vessel: the left anterior descending to the anteroseptal wall, the first diagonal branch to the anterolateral wall, the first obtuse marginal branch to the anterolateral wall, the second and third obtuse marginals to the posterior or posterior-lateral wall, and the right coronary artery to the posterior or posteroseptal wall.
The 13 injections in the right coronary artery opacified 21.1±6.1% (range, 10% to 32%) of the left ventricular myocardium. The 15 obtuse marginal branch injections opacified 19.1±5.1% (range, 11% to 28%) of the left ventricular myocardium. The 7 left anterior descending or diagonal branch injections opacified 36.9±7.0% (range, 28% to 46%) of the myocardium.
Posterior Papillary Muscle Perfusion
The posterior papillary muscle was opacified in 16 patients, 11 from the right coronary graft and 5 from the second or third obtuse marginal branch of the left circumflex coronary artery (see Fig 1⇓). In 10 of 16 patients (63%), the papillary muscle was perfused by one vessel (the right coronary artery in 8 patients and third obtuse marginal branch in 2). In 6 of 16 patients (37%), graft injection was followed by incomplete opacification involving either the septal half (3 right coronary injections) or the lateral half (3 second obtuse marginal injections) of the muscle. In these patients, the blood supply to the papillary muscle was considered to be double. In 2 patients, right coronary injections opacified the posteroseptal wall but not the papillary muscle. In these patients, even though the right coronary artery was dominant, the papillary muscle was entirely perfused by the third obtuse marginal branch of the left circumflex coronary artery.
Anterior Papillary Muscle Perfusion
Fourteen graft injections resulted in opacification of the anterior papillary muscle, which was invariably perfused by the left coronary artery. Partial opacification from one coronary branch was present in 10 patients (71%), while total opacification occurred in only 4 patients (29%). The first obtuse marginal branch of the left circumflex coronary artery subserved the lateral aspect of the muscle in 6 patients and the entire muscle in 2 patients. The first diagonal branch provided complete opacification in 2 cases and incomplete opacification in 4 cases. Two injections in the second obtuse marginal branch opacified the lateral wall but not the papillary muscle. The injection in the left anterior descending artery opacified the anteroseptal wall but not the papillary muscle.
Mitral Regurgitation Versus Posterior Papillary Perfusion and Inferior Infarction
The prevalence of inferior myocardial infarction was similar in the groups with single versus double vascular supply (P=NS). None of the patients with double perfusion had mitral regurgitation, while 60% of the patients with single perfusion had mild to moderate mitral regurgitation (P=.03). Mitral regurgitation affected only subjects with old inferior myocardial infarction and single blood supply to the posterior papillary muscle (P=.03). Patients with posterior myocardial infarction and double vascular supply had no mitral regurgitation. (See the Table⇓ and Fig 2⇓.)
No patient showed significant bleeding or vessel trauma at the site of graft injection. Myocardial washout of the agent ranged from three to seven cardiac cycles, and microbubble transit did not affect regional systolic function. PSWT in segments with old myocardial infarction was 9.2±3.5% before contrast appearance and 10.5±5.2% during myocardial opacification (P=NS), and in normal segments, PSWT was 40.9±11.4% before contrast and 39.0±12.8% during myocardial opacification (P=NS).
Partial or total rupture of a papillary muscle is a rare but often fatal complication of acute myocardial infarction. Wei et al9 estimated that this complication affects 0.5% to 5% of patients with acute myocardial infarction. Inferior wall infarction can lead to rupture of the posteromedial papillary muscle, which occurs more commonly than rupture of the anterolateral papillary muscle, secondary to anterolateral infarction. Unlike rupture of the interventricular septum, which is usually secondary to large infarcts, papillary muscle ruptures after relatively small infarctions in about 50% of the cases.17
Most studies on papillary muscle perfusion and dysfunction have been based on postmortem evaluation. Extensive anatomic studies on the microvasculature of the papillary muscles were reported in 1885 from the Anatomic Academy of Florence1 2 and later by Gross,3 Spalteholz,4 and Esthes et al.7 Spalteholz and Esthes et al focused on the precarious architecture of papillary microcirculation, consisting of long perforating branches originating directly from the epicardial vessels and entering the papillary muscle radially to join a large subendocardial anastomotic network.
Microvascular architecture appears to explain the focal or diffuse fibrosis, probably due to chronic, diffuse subendocardial ischemia,34 observed in the elderly. Conversely, the anastomotic network may have a protective role in the survival of papillary muscle after myocardial infarction if blood supply is provided by two coronary arteries rather than one.
Spalteholz4 first pointed out the variability of posterior papillary muscle blood supply. He found that a left dominant coronary artery may or may not perfuse the posterior papillary muscle, while a right dominant coronary artery invariably perfuses the muscle. The anterolateral papillary muscle was usually supplied by marginal tributaries from the left circumflex coronary artery.
Autopsy studies are performed in nonphysiological conditions using intra-aortic or intracoronary injections of barium sulfate for 20 minutes. This method allows detailed visualization of the coronary tree, including the microvasculature. However, the presence of extensive subendocardial papillary anastomoses obstructs the distinction between single and double vascularization.
Echocontrast agents with rheological behavior similar to that of red blood cells32 33 allow the in vivo study of myocardial perfusion with the high spatial and temporal resolution of ultrasonic imaging. The microbubbles are strong ultrasound reflectors, and during their microvascular transit in the myocardium, they produce a clear-cut contrast effect, thus allowing in vivo measurement, under physiological conditions, of the myocardial “area at risk.”21 25 28
Myocardial contrast echocardiography has been used during cardiac catheterization to study posterior papillary muscle perfusion.18 However, coronary artery bypass grafting with superselective contrast injections is an ideal model to study the distribution of coronary blood flow to the myocardium and to the papillary muscles. Since normal blood flow is restored by surgery, the biasing effect of collateral circulation is prevented.
Our study provides an explanation for the higher prevalence of posterior papillary muscle dysfunction after myocardial infarction. In the majority of our patients, the posterior papillary muscle, along with the posterior wall, was entirely perfused either by the right coronary artery or by the third obtuse marginal branch. Moreover, inferior myocardial infarction produced mitral regurgitation only in patients with blood supply from a single coronary vessel.
Conversely, the anterior papillary muscle was more often perfused by two separate arteries, the first obtuse marginal, originating from the left circumflex, and the first diagonal branch, originating from the left anterior descending. When one of the two arteries is occluded, the collateral flow from the patent vessel may prevent dysfunction.
In our study, and in partial contrast with Spalteholz,4 the right dominant coronary artery did not invariably perfuse the posterior papillary muscle: in two cases, the posteroseptal wall was opacified without involvement of the papillary muscle. This finding indicates the need to reconsider the significance of coronary artery dominance and may also have important clinical implications in the assessment of myocardial viability during acute myocardial infarction.35 36 37
This study was supported in part by Consiglio Nazionale delle Ricerche grant 92.03587.CT04, Rome, Italy. The authors are grateful to Paolo Merialdo, Civil Engineer, for assistance in image processing and to Flavia Chiarotti for statistical analysis.
Reprint requests to Dr Paolo Voci, Institute of Cardiac Surgery, “La Sapienza” University of Rome, Via S Giovanni Eudes, 27 00163 Rome, Italy.
- Received August 16, 1994.
- Revision received October 5, 1994.
- Accepted October 14, 1994.
- Copyright © 1995 by American Heart Association
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