Original Article
Enhanced Detection of Ischemic but Viable Myocardium by the Reinjection of Thallium after Stress-Redistribution Imaging
N Engl J Med 1990; 323:141-146July 19, 1990
- Abstract
- Abstract
Background.
The identification of ischemic but viable myocardium by thallium exercise scintigraphy is often imprecise, since many of the perfusion defects that develop in ischemic myocardium during exercise do not "fill in" on subsequent redistribution images. We hypothesized that a second injection of thallium given after the redistribution images were taken might improve the detection of ischemic but viable myocardium.
Methods.
We studied 100 patients with coronary artery disease, using thallium exercise tomographic imaging and radionuclide angiography. Patients received 2 mCi of thallium intravenously during exercise, redistribution imaging was performed three to four hours later, and a second dose of 1 mCi of thallium was injected at rest immediately thereafter. The three sets of images (stress, redistribution, and reinjection) were then analyzed.
Results.
Ninety-two of the 100 patients had exercise-induced perfusion defects. Of the 260 abnormal myocardial regions identified by stress imaging, 85 (33 percent) appeared to be irreversible on redistribution imaging three to four hours later. However, 42 of these apparently irreversible defects (49 percent) demonstrated improved or normal thallium uptake after the second injection of thallium, with an increase in mean regional uptake from 56± 12 percent on redistribution studies to 64± 10 percent on reinjection imaging (P<0.001). Twenty patients were restudied three to six months after coronary angioplasty. Of the 15 myocardial regions with defects on redistribution studies that were identified as viable by reinjection studies before angioplasty, 13 (87 percent) had normal thallium uptake and improved regional wall motion after angioplasty. In contrast, all eight regions with persistent defects on reinjection imaging before angioplasty had abnormal thallium uptake and abnormal regional wall motion after angioplasty.
Conclusions.
These data indicate that the reinjection of thallium improves the detection of ischemic myocardium and that myocardial regions with improved thallium uptake on reinjection imaging represent viable but jeopardized myocardium. (N Engl J Med 1990; 323:141–6.)
Media in This Article
Figure 1
Sector Analysis for Assessing the Regional Uptake of Thallium by the Myocardium.Figure 2
Short-Axis Thallium Tomograms during Stress, Redistribution, and Reinjection Imaging in a Patient with Coronary Artery Disease.Article Activity
- Article
IN many patients with coronary artery disease, impaired left ventricular systolic function at rest is caused by regionally ischemic or "hibernating" myocardium rather than irreversibly damaged myocardium.1 , 2 In such patients, left ventricular function will improve after revascularization.3 4 5 6 However, the identification of patients with such potentially reversible left ventricular dysfunction has been difficult.
Myocardial perfusion imaging with thallium-201 is a clinically important adjunct to exercise testing for the evaluation of patients with coronary artery disease.7 , 8 Thallium imaging is of value in detecting viable myocardium when regions with perfusion defects during exercise (stress imaging) demonstrate "redistribution" of the isotope on images obtained three to four hours later at rest (redistribution imaging). In many regions of viable myocardium, however, defects that are detected during thallium exercise testing persist and appear to be irreversible on images taken at rest three to four hours later.9 10 11 Thus, standard thallium scintigraphy may not always distinguish between regions of infarcted or ischemic myocardium in patients with left ventricular dysfunction.
The redistribution of thallium ("filling in") in a given defect may depend not only on the severity of the perfusion abnormality detected during exercise testing, but also on the subsequent levels of thallium in the blood. We hypothesized that the reinjection of thallium immediately after redistribution imaging might augment the blood concentration of the isotope to facilitate myocardial uptake in such viable regions. Thus, reinjection would provide an opportunity to compare relative perfusion under stress and resting conditions.
Methods
Selection of Patients
We studied 100 patients with coronary artery disease. A history and chest x-ray film were obtained for all patients, and all patients underwent physical examination, electrocardiography, coronary arteriography, radionuclide angiography, and exercise thallium single-photon-emission computed tomography (SPECT). Coronary artery disease was defined as a reduction ≥50 percent in the luminal diameter of at least one major epicardial coronary artery as determined by coronary angiography. All cardiac medications were withdrawn before exercise studies in 66 percent of the patients. These protocol studies were approved by the Institutional Clinical Research Subpanel of the National Heart, Lung, and Blood Institute, and all patients gave informed consent. We studied only patients with chronic stable coronary artery disease; no patient with recent acute myocardial infarction or unstable angina was included in the study. Twelve patients had undergone coronary-artery bypass surgery previously. The patients ranged in age from 26 to 79 years (mean, 58); there were 88 men and 12 women. The selection of patients for this reinjection protocol was performed without knowledge of the patients' coronary anatomy, left ventricular function, or the results of conventional stress-redistribution thallium imaging.
Exercise Thallium SPECT
After an overnight fast, the patients underwent thallium scintigraphy while exercising on a treadmill according to a standardized multistage exercise-test protocol, with continuous monitoring of symptoms, electrocardiogram, heart rate, and blood pressure. During exercise, 64 percent of the patients had an increase in their heart rate to more than 85 percent of the maximal predicted rate. At peak exercise, 2 mCi of thallium-201 was administered intravenously, and the patient continued to exercise for an additional 45 to 60 seconds. Thallium images were then obtained with a wide-field-of-view rotating gamma camera equipped with a high-sensitivity, low-energy, medium-resolution, parallel-hole collimator (Apex 415, APC-3, Elscint, Boston) centered on the 68-keV photo peak with a 20 percent window. The camera was rotated in a 180-degree arc in an elliptical orbit about the patient's thorax from a right-anterior oblique angle of 40 degrees to a left-posterior oblique angle of 40 degrees at 6-degree increments for 30 seconds each. Redistribution images were obtained three to four hours after exercise testing while the patients were resting. Immediately thereafter, all patients received a second injection of 1 mCi of thallium-201, and SPECT was performed within 10 to 15 minutes (reinjection imaging). From the raw scintigraphic data, sagittal, short-axis, and long-axis tomograms were reconstructed as previously described,12 and four consecutive representative slices of each view were selected for interpretation. The reconstructed stress, redistribution, and reinjection images were then analyzed both qualitatively and quantitatively.
Qualitative Thallium Analysis
The distribution of thallium uptake was analyzed qualitatively in the three tomographic views (four slices per view) as follows: the septal, apical, and lateral regions in the long-axis (transaxial) view; the anterior, apical, and inferior regions in the sagittal view; and the anterior, septal, inferior, and lateral regions in the short-axis (oblique) view. The stress, redistribution, and reinjection images were standardized to the maximal myocardial activity in the stress images and paired for simultaneous display: stress and redistribution images, stress and reinjection images, and redistribution and reinjection images. The resulting 300 paired images were displayed in random order and graded by two experienced, blinded observers using a three-point scale, on which 0 indicated markedly reduced or absent activity, 1 definitely reduced activity, and 2 normal activity. The grade assigned to a given region was the lowest regional score from all tomographic slices and views.
Quantitative Thallium Analysis
The thallium images were also analyzed with a semiautomatic quantitative circumferential-profile analysis applied to the short-axis tomograms. Briefly, for each patient, an operator-defined region of interest was drawn around the left ventricular activity of each short-axis slice on the stress images and the corresponding tomograms of the redistribution and reinjection images. The myocardial activity was subdivided into 64 sectors, each emanating from the center of the tomograms. All 64 sectors were of equal arc, which began at 3 o'clock (the middle of the lateral wall) and proceeded counterclockwise (Fig. 1Figure 1
Sector Analysis for Assessing the Regional Uptake of Thallium by the Myocardium.). The mean counts per pixel within the myocardial sectors of the redistribution and reinjection images were standardized to the sector with greatest thallium activity in the stress images. To facilitate comparison of these data with the qualitative interpretations, the sectors were then grouped and averaged into four myocardial regions (Fig. 1). Thus, for the 100 patients a total of 400 regions were evaluated.To determine the normal range for analysis of the quantitative data, we also studied 50 normal subjects (26 men and 24 women) who had no evidence of cardiovascular or pulmonary disease and whose physical examinations, electrocardiograms, and echocardiograms were normal. A myocardial region was considered abnormal in a patient with coronary artery disease if the thallium uptake on the stress image was more than 2 SD below the mean for the same region in the normal subjects of the same sex. Reproducibility studies were performed in 40 patients to determine the precision of measurement for assessing changes in thallium activity in each myocardial region among the stress, redistribution, and reinjection studies. A region with reduced activity on the stress study was considered irreversibly abnormal if the increase in the standardized thallium activity in that region did not exceed the reproducibility limit for that region on subsequent images. Alternatively, a region with reduced activity on the stress study was considered reversibly ischemic if the increase of standardized thallium uptake on the redistribution or reinjection image exceeded the reproducibility limit for that region. Similarly, regional thallium "washout" was defined as a decrease in relative thallium activity between the redistribution and reinjection images that exceeded the reproducibility limit for that region.
Gated Blood-Pool Cardiac Scintigraphy
Radionuclide angiography was performed to assess the left ventricular ejection fraction and regional wall motion at rest, with the use of red cells labeled in vivo with 15 to 20 mCi of technetium-99m. Imaging was performed with a conventional Anger camera equipped with a high-sensitivity parallel-hole collimator, as previously described.13 The left ventricular ejection fraction was derived by computer analysis of the scintigraphic data, and regional wall motion was assessed qualitatively by two experienced observers from the images displayed in cineangiographic format.13 With our technique, the lower limit of normal for the resting ejection fraction is 45 percent, with a reproducibility limit of 4 percent.14 The left ventricular ejection fraction in the 100 patients ranged from 16 to 69 percent (mean, 44± 12 percent) and was below the normal range in 50 patients.
Coronary Arteriography
Cardiac catheterization was performed within one to two weeks of the thallium studies in 85 of the patients and within a mean of six months in the other 15; we used the percutaneous femoral technique. Coronary-artery stenosis and graft patency were assessed by experienced cardiologists without knowledge of the results of thallium exercise testing or radionuclide angiography. Thirty-nine patients had marked narrowing of one vessel, 26 of two vessels, and 35 of three vessels. In patients with bypass grafts, a vessel was considered patent if there was no important narrowing (<50 percent) in the graft or in the native coronary artery distal to the graft anastomosis.
Percutaneous Transluminal Coronary Angioplasty
Twenty of the 100 patients underwent percutaneous transluminal coronary angioplasty according to the procedure initially described by Grüntzig and coworkers.15 Immediate improvement in coronary-artery stenosis was assessed angiographically by measuring the luminal diameter and directly by measuring the transstenotic coronary-artery-pressure gradient. Three to six months after revascularization, these patients again underwent thallium exercise SPECT, radionuclide angiography, and coronary angiography to assess vessel patency.
Statistical Analysis
The quantitative regional uptake of thallium during stress, redistribution, and reinjection imaging, standardized for peak activity during the stress study, was analyzed with the two-tailed paired t-test. The absolute quantitative uptake of thallium in regions with apparent washout as compared with normal regions was analyzed with the two-tailed unpaired t-test.
Results
During thallium exercise testing, perfusion defects developed in 92 of the 100 patients, whereas the remaining 8 patients had homogeneous regional uptake of thallium. Among the 92 patients with exercise-induced defects, a total of 260 myocardial regions (2.6 regions per patient) were graded as abnormal by qualitative analysis, and 259 regions were abnormal by quantitative analysis.
Qualitative Thallium Analysis
Of the 260 myocardial regions that were considered to be abnormal on the stress images, 88 (34 percent) were considered to be completely normal on the conventional redistribution images, and the other 172 (66 percent) were considered to have persistent defects. Eighty-seven of the persistent abnormalities identified by stress imaging were partially reversed on redistribution imaging, and 85 remained irreversible (or "fixed").
After the reinjection of thallium, thallium uptake increased in 42 of the 85 regions with fixed defects (49 percent) — a response suggestive of viable myocardium — and uptake was completely normal in 23 of the 42 regions. An example of the divergent results for the three measurements is shown in Figure 2Figure 2
Short-Axis Thallium Tomograms during Stress, Redistribution, and Reinjection Imaging in a Patient with Coronary Artery Disease.: stress imaging and redistribution imaging indicate apparently fixed anterior and septal defects, whereas reinjection imaging indicates normal perfusion in these areas. The 85 fixed defects identified by redistribution imaging were observed in a total of 43 patients, of whom 27 (63 percent) had improved thallium uptake on reinjection imaging. Fixed defects occurred more frequently in patients with left ventricular dysfunction: 31 of the 43 patients (72 percent) had subnormal ejection fractions. Thallium uptake improved on reinjection imaging in 20 of the 31 patients (65 percent).Of the 87 regions determined by stress imaging to have abnormal perfusion that was only partially reversed on redistribution imaging, 49 (56 percent) had further increases in thallium uptake on reinjection imaging; in fact, 45 of the 49 (92 percent) had normal perfusion. Thus, 101 of the 172 regions with persistent defects that were identified as either fixed or only partially reversible on redistribution imaging demonstrated enhanced thallium uptake on reinjection imaging. Reinjection imaging identified 46 patients with reversible abnormalities of thallium perfusion that would have been considered fixed or only partially reversible on standard redistribution imaging. These results were the same whether or not the patients were studied while taking antianginal medications.
Quantitative Thallium Analysis
Of the 259 myocardial regions identified as having perfusion abnormalities by stress imaging, 115 (44 percent) were identified as having fixed defects by redistribution imaging. Reinjection imaging showed that 46 of the regions with apparently fixed defects (40 percent) had improved or normal thallium uptake, with an increase in mean regional uptake from 58±13 percent during redistribution imaging to 71±13 percent during reinjection imaging. An example of increased regional thallium activity after reinjection imaging in one patient is shown in Figure 3Figure 3
Quantitative Analysis of Regional Thallium Activity.. In contrast, in 69 regions identified by reinjection imaging to have persistent defects, the mean regional uptake of thallium remained unchanged (redistribution imaging, 61±14 percent; reinjection imaging, 62±14 percent).This quantitative method was then applied to the 42 regions with fixed defects according to redistribution-imaging criteria that were judged to be viable after reinjection imaging on the basis of qualitative analysis. Enhanced thallium uptake on reinjection imaging was confirmed by quantitative analysis; the mean regional uptake of thallium increased from 56±12 percent during redistribution imaging to 64±10 percent during reinjection imaging (P<0.001). In contrast, in regions that were judged to have persistent perfusion defects on reinjection imaging on the basis of qualitative analysis, the mean regional uptake of thallium was similar during redistribution imaging and reinjection imaging (46± 14 percent vs. 47±12 percent; P not significant).
Apparent thallium washout between the redistribution and reinjection studies was observed in 27 of the 259 (10 percent) regions initially deemed abnormal. In 13 of these (5 percent), the regional interpretation was changed from reversible on redistribution imaging to fixed on reinjection imaging when compared with the results obtained during stress imaging. This apparent washout was caused by a disproportionate increase in thallium activity on reinjection imaging in the normal regions (51±5 percent increase) as compared with the ischemic regions (34±7 percent increase; P<0.01), producing the appearance of reduced activity in ischemic regions relative to that in normal regions. All 27 regions with apparent washout were served by critically narrowed coronary arteries (>75 percent stenosis); there was total occlusion of 14 regions.
Effects of Coronary Angioplasty
Among the 20 patients studied before and after percutaneous transluminal coronary angioplasty, there were 23 regions with persistent defects on redistribution imaging before angioplasty (either fixed or partially reversible abnormalities), of which 15 (65 percent) had enhanced thallium uptake on reinjection imaging. On repeat imaging three to six months after angioplasty, the uptake of thallium was normal on both stress and redistribution imaging in 13 of these 15 regions. Four of the 15 regions were considered to have completely fixed perfusion defects on redistribution imaging before revascularization; all 4 regions had normal thallium uptake after angioplasty. The improved thallium uptake on stress imaging in these 13 regions after angioplasty was associated with improved regional wall motion at rest on the basis of radionuclide angiography. In contrast, all eight regions with persistent defects on reinjection imaging before angioplasty again demonstrated persistent perfusion defects after angioplasty that were associated with persistent abnormalities in regional wall motion (P<0.001 by chi-square analysis).
Discussion
Thallium scintigraphy has played an important part in distinguishing ischemic from infarcted myocardium in patients with coronary artery disease. Since the uptake of thallium by the myocardial cell is an active process and depends on regional blood flow, it can be used as an index of both regional perfusion and myocardial viability.
In the initial clinical studies with thallium-201, two separate injections were used: one during maximal exercise and the other at rest. Because of the long half-life of thallium-201 and the resultant high levels of residual myocardial activity, the rest and exercise studies were performed one to two weeks apart. In 1977, Pohost and coworkers reported that perfusion defects identified by imaging immediately after exercise may disappear, or the thallium may be "redistributed," if imaging is repeated several hours after the exercise study.16 Several subsequent studies in animals showed that the redistribution noted when imaging was delayed represented an absolute reduction in thallium concentration in the normal segments along with an absolute increase in the concentration in ischemic segments.16 17 18 In clinical studies, initially reduced thallium uptake (after exercise) that is redistributed on images obtained after a delay of three to four hours is considered to represent ischemic myocardium. However, many exercise-induced perfusion defects in ischemic myocardium do not return to normal on redistribution imaging, even when the underlying myocardium is viable rather than infarcted.9 10 11 A possible explanation is that thallium redistribution in a given defect depends not only on the severity of the initial defect, but also on the continuing delivery of thallium over the subsequent three to four hours, as reflected by blood thallium levels. If the blood thallium level remains the same (or increases slightly) during the serial-imaging interval, an apparent defect that is actually viable myocardium should fill in; on the other hand, if the blood level continues to decrease, the delivery of thallium may be insufficient, and the defect may persist even though the underlying myocardium is not infarcted. These latter "irreversible" defects might be reversible if the delivery of thallium were augmented. Therefore, we hypothesized that the reinjection of thallium in patients at rest immediately after conventional redistribution imaging, performed three to four hours after exercise testing, would provide the necessary blood thallium concentration for uptake by viable yet compromised myocardium with apparently irreversible defects.
The reinjection of thallium in our patients significantly improved our ability to detect ischemic but viable myocardium in 49 percent of the regions that were interpreted as having irreversible, fixed abnormalities on redistribution imaging. The reinjection of thallium also enhanced the uptake of the isotope in 56 percent of the regions identified as having partially reversible defects by redistribution imaging. Thus, reinjection imaging identified as viable 101 of the 172 regions that conventional stress—redistribution imaging had identified as having persistent perfusion defects, greatly overestimating the extent and severity of myocardial fibrosis. Although apparent thallium washout was also observed between redistribution imaging and reinjection imaging in 10 percent of the abnormal myocardial regions, the relative washout changed the interpretation of the defects from reversible to fixed in only 5 percent of the regions. This phenomenon appears to be caused by a disproportionately smaller increment in regional thallium activity after reinjection in some ischemic regions as compared with normal regions. Thus, the washout effect reflects the reduction in regional perfusion at rest in regions served by critically stenosed or occluded coronary arteries, rather than differences in the rates of regional thallium clearance. In view of this point, we believe that the term "differential uptake" is preferable to "washout" to describe the phenomenon. Unlike conventional redistribution imaging, in which washout reflects an actual net loss of thallium activity between stress imaging and redistribution imaging, differential uptake after reinjection indicates a smaller accumulation of thallium in abnormal regions than in normal regions.
In 1978, Blood and associates reported discordance between conventional images obtained several hours after exercise and images obtained with thallium injected at rest.19 In their series of patients with coronary artery disease, perfusion defects were present in 56 percent on redistribution imaging, in contrast to only 32 percent on imaging performed after the injection of thallium under resting conditions (P<0.01). In 17 patients with discordant results, 16 had defects on conventional redistribution imaging but not on imaging performed at rest. A similar discordance between images obtained four to five hours after exercise and images obtained after thallium administration at rest was observed by Ritchie and coworkers.20 Kiat and coworkers reported that 61 percent of the segments with fixed defects on conventional delayed imaging demonstrated late redistribution when a third scan was obtained 18 to 72 hours after exercise.11
Our results are in agreement with these studies, in that nearly 50 percent of the regions with fixed defects on conventional redistribution imaging had further uptake of thallium after reinjection imaging at rest. More recently, Brunken and associates reported preservation of metabolic activity, as assessed by [18F]fluorodeoxyglucose uptake on positron-emission tomography, in 47 percent of myocardial segments with fixed defects and 64 percent of segments with partially reversible defects according to redistribution imaging with thallium.21 Our findings after reinjection imaging with thallium are remarkably similar to those obtained by fluorodeoxyglucose imaging, in that 49 percent of the fixed defects and 56 percent of the partially reversible defects identified by conventional redistribution imaging demonstrated enhanced thallium uptake after reinjection imaging at rest. Our conclusion that myocardial regions identified by thallium-reinjection imaging at rest represent viable myocardium is supported in the small subgroup of patients undergoing revascularization by the improvement in regional thallium uptake during exercise after angioplasty and the associated improvement in resting regional wall motion. Given the small number of patients studied after angioplasty, these results of revascularization must be considered preliminary until confirmed by a larger series.
Our results and those of the studies cited demonstrate that conventional redistribution imaging with thallium will incorrectly identify a considerable percentage of myocardial segments as being irreversibly injured. Although other methods have been shown to identify viable myocardium within such "irreversible" defects,11 , 21 there are practical considerations that may limit their routine application. Positron-emission tomography is very expensive and at present not readily available. Thallium imaging performed 18 to 72 hours after exercise is inconvenient, and the quality of the image is often poor. Our results suggest that reinjection imaging with thallium may provide a convenient, efficient, and accurate method of assessing myocardial viability in patients with otherwise fixed defects on thallium imaging in whom invasive interventions are contemplated for myocardial salvage.
We are indebted to Wendy R. Smeltzer and Ray Dextras for excellent technical assistance in the acquisition of the scintigraphic data.
Source Information
From the Cardiology Branch, National Heart, Lung, and Blood Institute, and the Department of Nuclear Medicine, National Institutes of Health, Bethesda, Md. (V.D., N.M.T.F., M.B.L., R.O.B.), and the West Roxbury Veterans Affairs Hospital, West Roxbury, Mass. (T.P.R). Address reprint requests to Dr. Dilsizian at the National Institutes of Health, Bldg. 10, Rm. 7B–15, Bethesda, MD 20892.
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