Original Article
An Association between Collateral Blood Flow and Myocardial Viability in Patients with Recent Myocardial Infarction
N Engl J Med 1992; 327:1825-1831December 24, 1992
- Abstract
- Abstract
Background.
We hypothesized that successful reperfusion of an occluded infarct-related coronary artery even late after acute myocardial infarction would result in improved regional wall motion and that such improvement might be related to the presence of collateral blood flow within the infarct bed.
Methods.
We assessed regional wall motion by two-dimensional echocardiography at base line and one month after angioplasty was attempted in the occluded infarct-related artery in 43 patients who had had a myocardial infarction two days to five weeks earlier. A wall-motion score was assigned to each patient on a five-point scale (from 1 [normal function] to 5 [dyskinesia]). The percentage of the infarct bed perfused by collateral flow was assessed with myocardial contrast echocardiography.
Results.
In the 41 patients who had abnormal wall motion at base line, improvement in function was noted in 25 (78 percent) of the 32 in whom angioplasty was successful, as compared with only 1 (11 percent) of the 9 in whom it was unsuccessful (P<0.001). The percentage of the infarct bed supplied by collateral flow at base line was directly correlated with wall function and inversely correlated with the wall-motion score one month after successful angioplasty (r = -0.64, P<0.001). Among the patients in whom angioplasty was successful, the 23 in whom >50 percent of the infarct bed was supplied by collateral flow had better wall motion (P<0.001) and greater improvement in wall motion at one month (P = 0.004) than the 9 in whom ≤50 percent of the bed was supplied by collateral flow. The degree of improvement in function was not influenced by the length of time between the infarction and the attempted angioplasty.
Conclusions.
The myocardium remains viable for a prolonged period in many patients with acute infarction and an occluded infarct-related artery. Viability appears to be associated with the presence of collateral blood flow within the infarct bed. (N Engl J Med 1992; 327:1825–31.)
Media in This Article
Figure 1
Short-Axis View of the Left Ventricle (LV) Obtained by Two-Dimensional Echocardiography in a Patient with an Occluded Right Coronary Artery.Figure 2
Correlation between the Wall-Motion Score One Month after Successful Angioplasty and the Mean (±SEM) Percentage of the Infarct Bed Supplied by Collateral Blood Flow at Base Line.Article Activity
- Article
BESIDES the amount of myocardium at risk, the two main determinants of both infarct size and the amount of viable myocardium after acute coronary occlusion are the duration of occlusion and the extent of collateral blood flow within the occluded vascular bed.1 , 2 Whereas the effect of the duration of coronary occlusion has been extensively studied,3 4 5 6 7 8 previous attempts to assess the importance of collateral vessels in patients with acute myocardial infarction have been limited by the techniques used.9 10 11 12 Coronary angiography, the method most often used to assess collateral blood flow, can identify only vessels greater than 100 μm in diameter,13 whereas most collateral vessels are smaller.14
We hypothesized that collateral blood flow to the infarct zone is common in patients with acute myocardial infarction. Consequently, successful reperfusion of an occluded infarct-related artery in such patients may result in improvement in regional function, and this improvement may be related to the extent of collateral blood flow within the infarct bed. Since adequate residual blood flow would maintain myocardial-cell viability for a prolonged period, we further hypothesized that the recovery of function may not be influenced by the duration of coronary occlusion.
To test these hypotheses, we performed a prospective study of patients with recent myocardial infarction and a totally occluded infarct-related artery. Myocardial contrast echocardiography was used to determine the extent of collateral blood flow to the infarct zone. In this procedure, microbubbles of air were injected directly into the coronary arteries in order to determine the spatial distribution of collateral blood flow within the myocardium.15 16 17 18 19 20 21 We also used this technique to determine the percentage of the left ventricular myocardium supplied by the infarct-related artery. Reperfusion of the infarct-related artery by means of coronary angioplasty was attempted.
Methods
Patients and Protocol
Fifty patients (33 men and 17 women; mean age, 56 years) with recent myocardial infarction (which had occurred two days to five weeks earlier) and a totally occluded infarct-related artery were included in the study. The decision to perform cardiac catheterization in these patients was made by the patients' primary physicians. Only nine (18 percent) of the patients had definite evidence of postinfarction ischemia, as documented by chest pain with associated electrocardiographic changes. Coronary angioplasty was attempted as part of the protocol, which was approved by the Human Investigation Committee at the University of Virginia, and all patients gave written informed consent. No patient with recent myocardial infarction who was found to have an occluded infarct-related artery was excluded from this study during the enrollment period.
Two-dimensional echocardiography was performed at base line. Myocardial contrast echocardiography was performed in the cardiac-catheterization laboratory just before angioplasty was attempted and was repeated after the last balloon inflation in patients in whom angioplasty was successful. Angioplasty was considered successful if anterograde flow was established in the infarct-related artery with a residual stenosis of less than 50 percent, and it was considered unsuccessful if anterograde flow was not reestablished or if reocclusion of an artery that had initially been treated successfully was documented by coronary angiography before hospital discharge. Two-dimensional echocardiography was repeated at one month in all patients, whether or not angioplasty was successful.
Coronary Angiography
The angiogram obtained before angioplasty was attempted was reviewed by two blinded observers who determined the presence or absence of multivessel disease and the extent of visible collateral vessels. Substantial coronary artery disease in arteries other than the infarct-related artery was defined as ≥50 percent narrowing of the luminal diameter of the proximal or middle portion of a major epicardial vessel or its major branches. The extent of perfusion by collateral vessels on angiography was scored as follows: 0, no collateral vessels seen; 1, some collateral vessels seen, with incomplete, delayed filling of the infarct-related artery; 2, well-formed collateral vessels seen, with delayed filling of the infarct-related artery; and 3, abundant collateral vessels seen that filled the infarct-related artery at the same rate as the artery being injected.
Myocardial Contrast Echocardiography
We have previously described the method of assessing collateral blood flow with myocardial contrast echocardiography.21 In brief, 1.5 ml of sonicated diatrizoate sodium—diatrizoate meglumine (Renografin-76, Squibb), which contains 500,000±200,000 microbubbles of air with a mean diameter of 6 μm,22 was injected first into the left main coronary artery and then into the right coronary artery before angioplasty, during simultaneously performed two-dimensional echocardiographic imaging at the mid—papillary-muscle level (short-axis view). We and others have demonstrated this procedure to be safe in humans.23 , 24
In patients in whom angioplasty was successful, microbubbles of air were selectively injected into the opened infarct-related artery to define the perfusion bed supplied by that vessel.21 This region was traced on a clear plastic overlay and expressed as a percentage of the left ventricular myocardium in that short-axis view. The overlay was then superimposed on the contrast echocardiogram obtained before angioplasty during the injection of microbubbles of air into the non—infarct-related artery to determine the percentage of the perfusion bed receiving collateral flow. Regions with any degree of contrast enhancement were distinguished from those with no enhancement. As we have previously reported, regions with less than 15 percent of normal flow do not demonstrate myocardial contrast enhancement after the intracoronary injection of sonicated diatrizoate sodium—diatrizoate meglumine.25
Figure 1Figure 1
Short-Axis View of the Left Ventricle (LV) Obtained by Two-Dimensional Echocardiography in a Patient with an Occluded Right Coronary Artery. shows a short-axis echocardiographic view after the injection of microbubbles of air into the left main coronary artery of a patient with an occluded right coronary artery. All regions of the myocardium show contrast enhancement, including that subtended by the occluded right coronary artery. Also shown in Figure 1 is the same view after the occluded right coronary artery was successfully opened by angioplasty (that is, after anterograde flow was established with <50 percent residual stenosis) and microbubbles of air were injected selectively into it to define the perfusion bed of the right coronary artery. It is apparent that before angioplasty, 100 percent of the perfusion bed of the right coronary artery was supplied by collateral blood flow.In the patients in whom angioplasty was unsuccessful (either no anterograde flow was established during the attempted angioplasty or reocclusion was documented before hospital discharge), the infarct zone was defined as the region with abnormal wall motion. We have previously shown that the size of the perfusion bed of a coronary artery correlates closely with the extent of abnormal wall motion when the artery is occluded.26 The region with abnormal motion was traced on a clear plastic overlay, and its extent was expressed as a percentage of the left ventricular myocardium in the short-axis view. The extent of collateral flow within this region was determined as described above. The interobserver and intraobserver variations in values obtained by our method are small.15
Two-Dimensional Echocardiography
Two-dimensional echocardiography was performed before and one month after angioplasty was attempted. Standard views of the left ventricle were obtained, and wall motion within the infarct bed was graded as follows: 1, normal function; 2, mild hypokinesia; 3, severe hypokinesia; 4, akinesia; and 5, dyskinesia.25 Scoring was carried out by two experienced observers who were blinded to all other information about the patients. The interobserver and intraobserver correlation with this method is good.27 Improvement in regional function after angioplasty was defined as a decrease of at least 1 in the wall-motion score.
Statistical Analysis
All data were expressed as means ±SEM. Data obtained in the same patient before and after angioplasty were compared with either paired Student's t-tests or chi-square tests; comparisons between groups were performed with either unpaired t-tests or Fisher's exact tests.28 Correlations of ordinal data were assessed with Spearman's rank statistic.28 Differences were considered statistically significant at a two-sided P value of <0.05.
Results
Clinical Characteristics
Of the 50 patients initially included in the study, 5 had technically inadequate echocardiographic data at base line because of poor acoustic windows, making it impossible to assess regional function adequately. Two patients did not return for study after angioplasty. Of the remaining 43 patients, 34 (79 percent) underwent successful angioplasty with no clinical evidence of reocclusion, whereas in 9 angioplasty was initially unsuccessful (n = 7) or angioplasty was successful but reocclusion was documented during the hospital stay (n = 2). There were no differences between patients in whom angioplasty was successful and those in whom it was unsuccessful in terms of base-line characteristics (Table 1Table 1
Base-Line Clinical Characteristics of Patients with Recent Myocardial Infarction (MI).*).Regional Wall Motion
In two patients, wall motion within the infarct region was normal at base line; in both, 100 percent of the infarct bed was supplied by collateral flow. Of the remaining 41 patients, wall motion in the infarct region had improved by at least one grade at one month in 25 (78 percent) of the 32 in whom angioplasty was successful, as compared with only 1(11 percent) of the 9 in whom the procedure was unsuccessful (P<0.001). Although the mean wall-motion score was essentially the same in both groups before angioplasty (3.1±0.2 for patients with successful angioplasty vs. 3.3±0.2 for those with unsuccessful angioplasty, P = 0.50), one month later it had improved significantly in those in whom angioplasty was successful (1.9±0.2) but not in those in whom it was unsuccessful (3.6±0.03, P<0.001).
Collateral Flow Measured by Myocardial Contrast Echocardiography
The percentage of the infarct bed supplied by collateral flow was similar in patients in whom angioplasty was successful and patients in whom it was unsuccessful (73±5 percent vs. 67±14 percent, P = 0.58). Since the mean score for regional function improved only in the group that underwent successful angioplasty, the relation between regional function and collateral flow was examined in the 32 patients in this group who had abnormal wall motion at base line. For these patients, there was a significant inverse correlation (r = -0.64, P<0.001) between the percentage of the infarct bed supplied by collateral flow at base line and the wall-motion score one month later (Fig. 2Figure 2
Correlation between the Wall-Motion Score One Month after Successful Angioplasty and the Mean (±SEM) Percentage of the Infarct Bed Supplied by Collateral Blood Flow at Base Line.). This correlation was essentially unchanged (r = -0.66, P<0.001) when the 10 patients with multivessel disease, a previous infarction, or both were excluded from the analysis.As Figure 3Figure 3
Mean (±SEM) Wall-Motion Score in Patients with Good and Poor Collateral Blood Flow on Myocardial Contrast Echocardiography. shows (left panel), the wall-motion score within the infarct zone was not significantly different at base line in the 23 patients in whom >50 percent of the bed was supplied by collateral flow and in the 9 in whom ≤50 percent was supplied by collateral flow (P = 0.18). The wall-motion score was significantly lower than the base-line score one month after successful angioplasty in the group with more extensive collateral flow (3.0±0.2 vs. 1.6±0.2, P<0.001), whereas it did not change significantly in the group with less extensive collateral flow (3.4±0.2 vs. 2.9±0.3, P = 0.14). Consequently, as Figure 3 shows (right panel), the change in the wall-motion score within the infarct bed was significantly greater in those in whom >50 percent of the infarct bed was supplied by collateral flow than in those in whom ≤50 percent of the bed was supplied by such flow (1.4±0.2 vs. 0.6±0.2, P = 0.004).The extent of the perfusion of myocardium by the infarct-related artery, expressed as a percentage of the left ventricular short-axis image, was similar in patients in whom ≤50 percent of the infarct bed was supplied by collateral flow and in those in whom >50 percent was so supplied (32±2 percent vs. 31±4 percent, P = 0.70). The size of the perfusion bed was not correlated with the percentage of the bed supplied by collateral flow (r = 0.18), with the wall-motion score (r = 0.07), or with the degree of improvement in the score one month after successful angioplasty (r = 0.23).
Collateral Flow Measured by Angiography
The presence of collateral vessels on angiography did not correlate with either base-line wall motion or the change in wall motion in the patients who had abnormal wall motion at base line. There was poor correlation between the collateral-vessel grade on angiography and the wall-motion score one month after successful angioplasty (r = -0.24, P = 0.16). The 15 patients with a low grade for collateral vessels (0 or 1) on angiography had the same mean base-line regional-wall-motion score as the 17 with good supply by collateral vessels (grade 2 or 3) (3.2±0.2 vs. 3.0±0.2, P = 0.37). The change in the wall-motion score after successful angioplasty was also similar for patients with angiographic evidence of poor or good supply by collateral vessels (1.1±0.3 vs. 1.2±0.1, P = 0.73). There was poor correlation between the percentage of the infarct bed supplied by collateral flow as determined by contrast echocardiography and the collateral-vessel grade on angiography (r = 0.05) in the 43 patients for whom data were analyzed. Seven of the nine patients in whom ≤50 percent of the infarct bed was supplied by collateral flow had good collateral blood supply (grade 2 or 3) on angiography.
Improvement in Wall Motion and the Duration of Coronary Occlusion
There was no relation between the probability and degree of improvement in wall motion and the interval between the myocardial infarction and the attempt at angioplasty (Table 2Table 2
Improvement in Regional Function after Angioplasty, According to the Length of Time between Acute Myocardial Infarction (MI) and Angioplasty.*). Seven (64 percent) of the 11 patients who underwent the procedure between two and seven days after myocardial infarction, 10 (77 percent) of the 13 who underwent angioplasty one to two weeks after infarction, and all of the 8 patients who underwent angioplasty two to five weeks after infarction had improvement in wall-motion score (P = 0.17). Substantial improvement occurred in all three groups, without any significant differences in the degree of improvement among the groups (P = 0.99).Discussion
This prospective study demonstrates that collateral-derived residual flow is present in many patients with a recent myocardial infarction and an occluded infarct-related artery. This blood flow maintains myocardial viability for a prolonged period despite total coronary occlusion, and restoration of anterograde blood flow as late as five weeks after myocardial infarction results in improvement in regional function even in patients with severe regional dysfunction, as long as they have adequate collateral flow at base line. Moreover, the degree of regional function after the restoration of anterograde flow is related to the percentage of the occluded bed perfused by collateral flow.
The Role of Collateral Blood Flow in Myocardial Infarction
That there is controversy about the importance of collateral blood flow in acute ischemic syndromes29 , 30 may be due in part to the methods used heretofore to assess collateral vessels in humans. Coronary angiography, the most frequently used diagnostic technique for the assessment of collateral vessels, has several limitations. It can identify only vessels >100 μm in diameter,13 although most arterial collateral vessels are smaller.14 Furthermore, although it can demonstrate the presence of epicardial collateral vessels, it does not specify the distribution of collateral flow within the myocardium.
Because of these limitations, the beneficial effects of angiographically identified collateral vessels on left ventricular function in patients who receive early reperfusion therapy during acute myocardial infarction have also become controversial. Saito et al.,9 Rentrop and coworkers,10 and Habib and colleagues11 reported beneficial effects of collateral vessels in such cases. Gohlke et al.,12 however, reported that the presence of collateral vessels did not protect against long-term adverse effects in patients with anterior Q-wave myocardial infarctions.
In this study, we have shown that the distribution of collateral blood flow within the occluded infarct bed is related to myocardial viability and that this distribution does not correlate with the collateral-vessel grade determined angiographically. Patients with poor collateral flow, as measured by myocardial contrast echocardiography, did not have improvement in regional function despite having good angiographic evidence of collateral vessels and despite undergoing successful angioplasty. The percentage of a perfusion bed supplied by collateral flow was also independent of the size of the perfusion bed itself. Thus, improvement in regional function after successful angioplasty was not limited to patients with infarct-related arteries that supply small perfusion beds.
It is generally believed that the improvement of regional function, the limitation of infarct expansion, and the prevention of heart failure and death are closely related to myocardial salvage, which can be achieved by reperfusion only in the first few hours after the onset of myocardial infarction.1 , 2 Our results indicate that substantial benefit may also be gained from reperfusion as late as five weeks after infarction in patients with persistent occlusion of the infarct-related artery, as long as collateral blood flow is present within the infarct bed.
The Value of Reperfusion Late after Myocardial Infarction
It is only recently that improved survival and better regional function have been reported in patients in whom patency of the infarct-related artery is restored late after myocardial infarction.31 32 33 34 35 36 A number of mechanisms have been suggested to explain the benefit of late reperfusion, including a decrease in fatal ventricular arrhythmias37 and the limitation of infarct expansion.38 , 39 A recent study by Topol and colleagues found that left ventricular dilatation was prevented at one month in patients who underwent late reperfusion.40 The lack of a persistent difference between treated and untreated patients after six months in that study may be due in part to the incomplete follow-up in a substantial proportion of patients, to coronary reocclusion in one fourth of the successfully treated patients, and to spontaneous recanalization in some untreated patients. Contrary to the mechanisms proposed above, our results suggest that late reperfusion may provide clinical benefit by improving the function of viable myocardium that is present within the infarct zone in most patients with acute myocardial infarction.
Limitations of the Study
Although there were no statistical differences in base-line characteristics between patients in whom angioplasty was successful and those in whom it was unsuccessful, our results are based on small numbers with wide confidence intervals; there is thus the potential for beta error. The extent to which the patients in our study represent an unselected population is also uncertain. The majority had single-vessel disease and thus did not have jeopardized collateral vessels. In addition, only one fifth of our patients had objective evidence of ischemia after infarction. We therefore believe that our results apply to a considerable number of patients with acute myocardial infarction.
In patients in whom angioplasty was successful, we did not repeat angiography one month later to determine whether the infarct-related artery was still patent. There were no clinical events to indicate reocclusion, however. We measured the size of the perfusion bed and the extent of collateral flow only in a single short-axis echocardiographic view, which may not have represented the topography of the entire infarct bed accurately. Some of the collateral vessels noted in our patients could have developed after the infarction, but their presence nonetheless indicates the presence of viable myocardium, since collateral growth usually occurs in response to tissue need.41 , 42 Therefore, we can report only an association, rather than a causal relation, between collateral blood flow and myocardial viability.
Clinical Implications
This study was not designed to assess the value of coronary angioplasty in patients with recent myocardial infarction and an occluded infarct-related artery. Instead, its purpose was to determine whether there was an association between improvement in regional function within an infarct bed after late reperfusion and the extent of collateral blood flow to that bed before reperfusion. Our data suggest that improvement in function after late reperfusion may explain the clinical benefit seen in other studies among patients in whom patency of the infarct-related artery was reestablished late after myocardial infarction.31 32 33 34 35 36 , 40 Our results do not, however, necessarily indicate that angioplasty should be performed in all patients with acute infarction who have an occluded infarct-related artery and adequate collateral blood flow. Randomized studies of the long-term effects of angioplasty in such patients will be required before this important question can be answered.
Supported in part by a Clinical Investigator Award to Dr. Kaul (K08-HL01833) and a FIRST Award (R29-HL38345) from the National Institutes of Health and by a grant-in-aid from the Virginia affiliate of the American Heart Association. Dr. Ragosta was the recipient of a fellowship training grant from the Virginia affiliate of the American Heart Association, and Dr. Kaul is an Established Investigator of the American Heart Association, Dallas.
Presented in part at the 64th Annual Scientific Session of the American Heart Association (Samuel Levine Young Investigators' Award Competition), Anaheim, Calif., November 11, 1991.
Source Information
From the Division of Cardiology, Department of Medicine, University of Virginia School of Medicine, Charlottesville. Address reprint requests to Dr. Powers at the Division of Cardiology, Box 158, University of Virginia, Charlottesville, VA 22908.
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