CLINICAL STUDY: MYOCARDIAL ISCHEMIA
Significance of reduced uptake of iodinated fatty acid analogue for the evaluation of patients with acute chest pain
Yuko Kawai, MD*,
Eriko Tsukamoto, MD ,
Yoichi Nozaki, MD*,
Koichi Morita, MD,
Masayuki Sakurai, MD* and
Nagara Tamaki, MD*,*
* Department of Cardiovascular Medicine, Hokko Memorial Hospital, Sapporo, Japan
Department of Nuclear Medicine, Hokkaido University, School of Medicine, Sapporo, Japan
Manuscript received October 3, 2000;
revised manuscript received July 24, 2001,
accepted August 20, 2001.
* Reprint requests and correspondence: Dr. Nagara Tamaki, Hokkaido University, School of Medicine, Department of Nuclear Medicine, Kita 15, Nishi 7, Sapporo, 060-8638, Japan
natamaki{at}med.hokudai.ac.jp
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Abstract
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OBJECTIVES
To assess whether 15-(p-[iodine-123] iodophenyl)-3-(R,S) methylpentadecanoic acid (BMIPP) imaging can identify previous ischemic areas, BMIPP SPECT was performed in patients with acute chest pain to compare its findings with those of technetium-99m–tetrofosmin (tetrofosmin) SPECT and coronary angiography.
BACKGROUND
Basic studies indicate that BMIPP can identify previous ischemia as reduced tracer uptake.
METHODS
This study prospectively enrolled 111 consecutive patients with acute chest pain without myocardial infarction. Tetrofosmin SPECT was performed at rest within 24 h after the last episode of chest pain. Coronary angiography and BMIPP SPECT were also performed on the following day.
RESULTS
Sixty-four of the 87 patients with coronary stenosis or spasm showed BMIPP abnormalities corresponding to the areas of coronary abnormalities (sensitivity 74%), whereas only 33 of them showed perfusion abnormalities (sensitivity 38%) (p < 0.001). Of the 24 patients without coronary stenosis or spasm, 22 showed normal BMIPP SPECT (specificity 92%), and 23 showed normal tetrofosmin SPECT (sensitivity 96%). Coronary stenosis was more often seen in the group with abnormal tetrofosmin/abnormal BMIPP (82%) and with normal tetrofosmin/abnormal BMIPP (69%) than in the group with normal tetrofosmin/normal BMIPP (36%) (p < 0.05). Coronary spasm was observed more often in the group with abnormal tetrofosmin/abnormal BMIPP (83%) and with normal tetrofosmin/abnormal BMIPP (90%) than in the group with normal tetrofosmin/normal BMIPP (27%) (p < 0.05). The extent and severity scores of tetrofosmin and BMIPP in the patients with organic stenosis were significantly higher than those of patients with no organic stenosis or spasm (p < 0.0001).
CONCLUSIONS
These data indicate that BMIPP SPECT may specifically identify previous ischemic lesions due to coronary stenosis or spasm in patients with acute chest pain.
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Abbreviations and Acronyms
| | BMIPP | = 15-(p-[iodine-123] iodophenyl)-3-(R,S) methylpentadecanoic acid | | ECG | = electrocardiogram or electrocardiographic | | LAD | = left anterior descending coronary artery | | LCx | = left circumflex coronary artery | | MI | = myocardial infarction | | PET | = positron emission tomography | | RCA | = right coronary artery | | SPECT | = single-photon emission computed tomography |
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Although an accurate diagnosis and prompt therapy are important for patients with acute coronary syndromes, the evaluation of acute chest pain has been difficult for many years. An iodinated fatty acid analogue, 15-(p-[iodine-123] iodophenyl)-3-(R,S) methylpentadecanoic acid (BMIPP) can assess fatty acid utilization in the myocardium. Basic studies have indicated that BMIPP imaging can identify previous severe ischemia as areas of reduced tracer uptake (1). Previous studies have indicated that BMIPP imaging may identify a persistent alteration of fatty acid utilization shortly after recovery of perfusion (2–4).
We hypothesized that BMIPP imaging shortly after chest pain may reflect a metabolic alteration as reduced tracer uptake. To assess whether BMIPP imaging can identify previous ischemic areas, BMIPP single-photon emission computed tomography (SPECT) was performed to compare its findings with those of perfusion SPECT in patients with acute chest pain.
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Methods
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Patients group (Table 1).
From January 1997 to December 2000, nearly 600 patients presenting with severe chest pain were admitted to our hospital. This study included 111 consecutive patients (80 men and 31 women, 63 ± 12 years old) who received technetium-99m–tetrofosmin SPECT (tetrofosmin) within 24 h after the last episode of chest pain. All patients also underwent BMIPP SPECT and coronary angiography. Patients with acute and previous myocardial infarction (MI) or those who had undergone coronary angioplasty or coronary artery bypass graft surgery were excluded. Tetrofosmin SPECT was performed before coronary angiography.
Study protocol.
Tetrofosmin SPECT at rest and the BMIPP study were performed within 0.7 ± 0.5 days (1 to 24 h) and 1.7 ± 1.5 days (1 to 5 days) after the disappearance of the last episode of chest pain, respectively. The BMIPP SPECT study was performed within two days after the perfusion study (98 patients on the next day and 13 patients two days later). All patients underwent coronary angiography within 1 to 4 days (mean 2.8 ± 1.2 days) after the last episode of chest pain. In addition, 45 patients without organic coronary stenosis had a spasm provocation test (5,6). After a control angiogram was obtained, 20 µg of ergonovine maleate was selectively injected into the coronary arteries, which were considered as having spasm from the electrocardiographic (ECG) findings on hospital admission. When coronary spasm was induced and did not resolve spontaneously, 2.5 mg of isosorbide dinitrate was infused into the coronary artery. The provocation test was judged as positive only when all of the following criteria were satisfied: total or subtotal coronary occlusion, significant ST-T segment changes on the ECG and onset of chest pain.
Data analysis.
The left ventricular myocardium was divided into 20 segments to visually score the tracer uptake in each SPECT study on a four-point grading system (7): 0 = normal uptake; 1 = slightly reduced; 2 = moderately reduced; and 3 = severely reduced. Scores of 2 and 3 were considered to be significant. The extent score was defined as the total number of the segments exhibiting deteriorating uptake. The severity score was defined as the total number of the defect score. The septal and anterior segments correspond to the left anterior descending coronary artery (LAD), the inferior and posterior segments correspond to the right coronary artery (RCA) and the lateral segments correspond to the left circumflex coronary artery (LCx). In all patients, the areas of abnormal coronary arteries and the reduced uptake of BMIPP were the same. Luminal stenosis  75% was defined as a significant lesion. In each patient, the segmental uptake of tetrofosmin and BMIPP SPECT was graded by consensus of three nuclear physicians and cardiologists who had no previous knowledge of the clinical data or coronary angiographic findings. This was a completely blinded method. The interobserver variability was 92%.
Statistical analysis.
A comparison of proportions was made by using the Fisher exact test. To calculate the sensitivity and specificity, the significance of differences between the groups was determined by using the McNemar test. Analysis of variance with the Bonferroni correction was used to assess the significance of differences between the patient groups. All values are shown as the mean value ± SD. In all tests, p < 0.05 was regarded as significant.
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Results
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Clinical findings (Table 2).
Abnormal ECG findings were more often seen in the BMIPP-abnormal patients (29%) than in the BMIPP-normal patients (13%) (p < 0.05). Abnormal ECG findings were as follows: ST-T segment elevation (n = 16, 64%), right or left bundle branch block (n = 6, 24%), paroxysmal atrial fibrillation (n = 2, 8%) and transient complete atrial ventricular block (n = 1, 4%). Reduced wall motion on echocardiogram was more often seen in the BMIPP-abnormal patients (33%) than in the BMIPP-normal patients (7%) (p < 0.001). However, no significant difference was observed between the BMIPP findings and the duration of chest pain.
SPECT findings (Table 3).
A regional abnormality was seen in 34 patients (30%) on tetrofosmin SPECT at rest and in 66 patients (59%) on BMIPP SPECT at rest (p < 0.05). In all patients, the reduced uptake of BMIPP corresponded to the areas with abnormal coronary arteries. Thirty-four patients with abnormal perfusion showed an abnormality on BMIPP SPECT (group A). Of the 77 patients with normal perfusion, 32 patients showed an abnormality on BMIPP SPECT (group B), whereas 45 had normal BMIPP SPECT images (group C). The extent and severity scores of BMIPP were significantly higher than those of tetrofosmin both in groups A and B.
Coronary angiographic findings (Table 4).
There were 66 patients with significant organic stenosis. The spasm provocation test was performed in 45 patients without organic coronary stenosis. Total or subtotal coronary occlusion due to spasm, with ST-T segment changes and chest pain, was seen in 21 patients (46%). None of the patients had spasm with complex coronary arteries. Spontaneous spasm was seen in four patients. The spasm was resolved in all patients by isosorbide dinitrate injection.
Of a total of 87 patients with organic stenosis or spasm, 64 showed BMIPP abnormalities corresponding to the areas with coronary disease (sensitivity 74%), whereas only 33 of them showed perfusion abnormalities (sensitivity 38%) (p < 0.001). In contrast, 22 and 23 patients with no organic stenosis or spasm showed no BMIPP or perfusion abnormalities, respectively (specificity 92% and 96%, respectively) (p = NS). In addition, coronary artery stenosis was more often seen in group A (82%) and group B (69%) than in group C (36%) (p < 0.01). Coronary spasm was often seen in group A (83%) and group B (90%), but not often in group C (27%).
The sensitivities of BMIPP and tetrofosmin for detecting LAD stenosis were 85% and 90%, respectively. The specificities were 80% versus 88%, respectively. The sensitivity for detecting LCx stenosis was 50% for both BMIPP and tetrofosmin, and the specificity was 75% for both. The sensitivity for detecting RCA stenosis was 80% for both BMIPP and tetrofosmin, and the specificity was 75% for both. There were no statistically significant differences among these values between the two tracers.
Coronary angiographic findings and SPECT scores (Table 5).
The extent and severity scores of BMIPP in the 66 patients with organic stenosis were significantly higher than those in the 24 patients with no stenosis or spasm (p < 0.01). Similarly, the extent scores of BMIPP in the 21 patients with spasm were significantly higher than those in the patients with no stenosis or spasm (p < 0.05). In addition, in the patients with organic stenosis, the extent and severity scores of BMIPP were significantly higher than those of tetrofosmin (p < 0.05). In contrast, the extent and severity scores of tetrofosmin in the patients with organic stenosis or spasm were not different from those of patients with no stenosis or spasm. Thus, reduced uptake of BMIPP was considered to be specifically related to the presence of organic stenosis or spasm.
Subgroup analysis.
Of the 111 patients, 29 were selected as the subgroup that underwent perfusion SPECT within only 6 h after the last episode of chest pain. There were 13 patients with coronary stenosis and 8 patients with coronary spasm. The remaining eight patients had no organic stenosis and no spasm. Six patients (21%) showed regional perfusion abnormalities on tetrofosmin SPECT, and 14 patients (48%) showed abnormalities on BMIPP SPECT. In patients with coronary artery stenosis or spasm, the extent and severity scores of BMIPP were higher than those of tetrofosmin SPECT. The sensitivity of BMIPP SPECT to detect coronary stenosis or spasm (66%) was significantly higher than that of tetrofosmin SPECT (29%) (p < 0.01). The specificity was 100% for both BMIPP and tetrofosmin SPECT.
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Discussion
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Our data show that abnormal tracer uptake on BMIPP images was occasionally observed even in patients who had no perfusion abnormality at rest and in patients with acute chest pain, particularly those with severe coronary stenosis or spasm on coronary angiography. The BMIPP abnormalities were related to wall motion and ECG abnormalities. These data indicate that abnormal BMIPP uptake may reflect recurrent and severe previous ischemia. Therefore, BMIPP may be used for "ischemic memory imaging" in patients with acute chest pain but no MI. The evaluation of patients admitted to emergency departments with possible ischemia and a nondiagnostic ECG (8,9) is of paramount importance for identification of acute ischemia or infarction, or both, as well as for risk stratification. Technetium-99m perfusion agents have been used for this purpose. Most reports have indicated that myocardial ischemia may be accurately identified by perfusion studies at rest (10–12). Kontos et al. (13) showed that early rest perfusion imaging was a powerful predictor of MI. In addition, this may accurately identify patients with acute chest pain but no MI.
The present study supports the previous reports showing abnormal perfusion at rest in patients with acute chest pain but no evidence of MI. However, myocardial ischemia may not be identified by rest perfusion studies alone. Other studies indicate the importance of stress perfusion imaging in patients with chest pain but normal perfusion at rest (14,15). In contrast, stress perfusion imaging may not be feasible, particularly in unstable patients. We hypothesized that metabolic imaging at rest may add diagnostic accuracy for identifying severe myocardial ischemia in these patients.
Value of metabolic imaging.
In the normal myocardium under aerobic conditions, 70% to 80% of the energy source of myocardial utilization is dependent on beta-oxidization of fatty acids. However, in ischemic conditions or in the state of heart failure, beta-oxidization in the mitochondria is immediately reduced (16–19). More importantly, alterations of fatty acid utilization may persist in the postischemic dysfunctional myocardium as "ischemic memory" (20). 11C-palmitate is a well-established positron emission tomographic (PET) tracer for providing myocardial fatty acid utilization. However, in some countries, only a limited number of institutions equipped with a PET camera and cyclotron can study myocardial metabolism in vivo. In the meantime, radio-iodinated fatty acid tracers have been developed to probe fatty acid utilization with conventional gamma cameras (21–23). BMIPP is one of the most commonly used clinical agents in Japan and some European countries because of its high extraction and retention in the myocardium (22).
In clinical use, one of the advantages of BMIPP imaging is the ability to visualize the damaged myocardium as areas of reduced tracer uptake (1,22,23). Less BMIPP uptake than perfusion SPECT is often observed in acute or old MIs (2,6,24,25). Such discordant BMIPP uptake is often seen early after the onset of MI (26), indicating severe metabolic damage in the myocardium. We previously reported that the areas of abnormal BMIPP uptake in the subacute phase were similar to those of perfusion defects in the acute phase of MI (27). BMIPP SPECT can also be applied to ischemic disease without MI. In previous reports, the degree of reduced BMIPP uptake correlated with the severity of coronary artery stenosis (28,29). Because the flow reserve was more limited, and ischemic attack occurred more frequently in the coronary artery with significant stenosis than in the coronary artery with moderate stenosis, fatty acid utilization may decrease more in myocardial regions supplied by coronary arteries with severe stenosis. Yamabe et al. (30) reported BMIPP SPECT findings in subtypes of effort angina pectoris. The detection rate of stenosed vessels by BMIPP SPECT was more sensitive in the worsening type than in the stable or new-onset type. In our current study, we have not classified the subtype of unstable angina. However, our study suggests that abnormal BMIPP uptake may be seen in the case of recent chest pain. Thus, a new angina episode may likely alter the BMIPP uptake. All of these data suggest that reduced uptake of BMIPP may be observed in the territories of coronary arteries with severe stenosis with a recent ischemic episode (Fig. 1).
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Figure 1 (A) Coronary arteriogram of a 65-year-old woman with effort angina. Severe stenosis is seen in the left anterior descending coronary artery (arrow). (B) Sequential tetrofosmin images. No significant abnormal perfusion is observed on the tetrofosmin images obtained at the time of hospital admission. However, the BMIPP images obtained on the next day show severely reduced uptake in the apex and anteroseptal regions.
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Coronary spasm.
Coronary spasm is one of the important origins of chest pain, particularly in Japan. A variant form of angina pectoris was seen at rest with ST segment elevation, as described by Prinzmetal et al. (31) in 1959. Patients with vasospastic angina had left ventricular dysfunction due to recurrent ischemia, even without coronary stenosis. In addition, coronary vasospasm sometimes may be the cause of sudden death (32). Therefore, an accurate diagnosis and prompt therapy are clinically important. The diagnosis of coronary spasm was provoked by intracoronary injection of ergonovine maleate or acetylcholine (33–35). This type of angina is not usually induced by exercise or dipyridamole. Thus, a routine stress perfusion study was not able to induce vasospastic angina.
However, because altered fatty acid utilization may be associated with repetitive ischemic episodes, BMIPP SPECT may hold promise for detecting coronary spasm. The present study has shown that coronary spasm was most often seen in patients with abnormal BMIPP uptake with normal perfusion at rest (group B). Nakajima et al. (36) and Watanabe et al. (37) also reported abnormal BMIPP uptake in the territories of coronary spasm in patients with coronary vasospasm. Our results may confirm their findings (Fig. 2).
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Figure 2 (A) Coronary angiogram of a 48-year-old woman with rest angina in the early morning. Seven days later, coronary angiography shows no significant stenosis in either coronary artery. After injection of ergonovine maleate into the right coronary artery, total spasm was provoked (left), with severe chest pain and electrocardiographic changes. After isosorbide dinitrate was injected, the spasm was completely resolved (right). (B) Series of rest tetrofosmin perfusion and BMIPP single-photon emission computed tomography images. No significant abnormal perfusion is observed on the rest tetrofosmin images at the time of hospital admission. However, the BMIPP images show reduced uptake in the inferior region on the next day.
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Study limitations.
Although tetrofosmin is available in emergency departments in a cold-kit form, BMIPP is limited because of its unavailability on an emergency basis. A BMIPP SPECT study was obtained on the next day of admission at earliest. In patients with mild ischemia, the alteration of fatty acid utilization may improve, to a certain degree, in the first several days after myocardial ischemia. However, abnormal BMIPP uptake was often seen in patients with acute chest pain despite normal perfusion, and this result was helpful for detecting previous myocardial ischemia. The frequency of abnormal BMIPP uptake (29%) was relatively low, which may be due to the definition of BMIPP uptake abnormality and patient selection. We defined abnormal BMIPP uptake only when the score was 2 to eliminate those with equivocal or mildly reduced uptake. We enrolled patients with a wide variety of chest pains. When only patients with unstable angina were selected, abnormal BMIPP uptake was more frequently observed.
Clinical implications.
In our study, abnormal BMIPP uptake was occasionally observed in patients with acute chest pain. Although a tetrofosmin study can identify patients with acute chest pain due to ischemia, rest perfusion studies may often show normal findings, despite severe coronary artery stenosis. In those patients, a stress test may be available to identify myocardial ischemia. However, not all patients with acute chest pain can undergo a stress test, especially elderly people or patients with unstable angina. In addition, even a stress test may not identify myocardial ischemia due to coronary spasm. In patients with chest pain, BMIPP SPECT is very useful for identifying severe ischemia at rest as areas of altered fatty acid utilization, before performing coronary angiography or a provocation test.
Conclusions.
Abnormal BMIPP uptake at rest was occasionally seen in ischemic regions in patients with acute chest pain. Fourteen percent of patients with acute chest pain showed abnormal BMIPP uptake with normal perfusion at rest. These patients were the most likely to have severe coronary stenosis and vasospasm on angiography. The BMIPP abnormalities were significantly related to wall motion and ECG abnormalities. This was probably due to prolonged impairment of fatty acid utilization, followed by repeated ischemic attacks, which may persist after the last episode of chest pain.
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Acknowledgments
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We deeply appreciate T. Kameya, T. Yamaguchi, T. Ueda, Y. Sato, H. Wakakuni, Y. Kondo, K. Akibayashi, K. Baba, Y. Tamura and S. Oikawa for their skilled technical assistance. We thank Drs. S. Ohta, K. Kishino, O. Yamada, A. Yotsukura, Y. Takagi, H. Tanaka and T. Horisaki for examining the patients. We also acknowledge Dr. T. Kohya and Prof. A. Kitabatake, at Hokkaido University, for their valuable comments.
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I. Carrio, M. R. Cowie, J. Yamazaki, J. Udelson, and P. G. Camici
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T. Asanuma, A. Uranishi, K. Masuda, F. Ishikura, S. Beppu, and S. Nakatani
Assessment of Myocardial Ischemic Memory Using Persistence of Post-Systolic Thickening After Recovery From Ischemia
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V. Dilsizian
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A. L. Baggish and C. A. Boucher
Radiopharmaceutical Agents for Myocardial Perfusion Imaging
Circulation,
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S. H. Rahimtoola, V. Dilsizian, C. M. Kramer, T. H. Marwick, and J.-L. J. Vanoverschelde
Chronic ischemic left ventricular dysfunction from pathophysiology to imaging and its integration into clinical practice.
J. Am. Coll. Cardiol. Img.,
July 1, 2008;
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T. Higuchi and F. M Bengel
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Heart,
June 1, 2008;
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M. R. Vesely and V. Dilsizian
Nuclear Cardiac Stress Testing in the Era of Molecular Medicine
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M. Nishimura, K. Tsukamoto, N. Hasebe, N. Tamaki, K. Kikuchi, and T. Ono
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V. Dilsizian and J. C. Fink
Deleterious Effect of Altered Myocardial Fatty Acid Metabolism in Kidney Disease
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V. Dilsizian, T. M. Bateman, S. R. Bergmann, R. Des Prez, M. Y. Magram, A. E. Goodbody, J. W. Babich, and J. E. Udelson
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Circulation,
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[Abstract]
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J E Udelson and E J Flint
Radionuclide imaging in risk assessment after acute coronary syndromes
Heart,
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S. Kurisu, I. Inoue, T. Kawagoe, M. Ishihara, Y. Shimatani, K. Nishioka, T. Umemura, S. Nakamura, M. Yoshida, and H. Sato
Myocardial perfusion and fatty acid metabolism in patients with tako-tsubo-like left ventricular dysfunction
J. Am. Coll. Cardiol.,
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[Abstract]
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Abstract
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