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Regional 11C-Hydroxyephedrine Retention in Hibernating Myocardium: Chronic Inhomogeneity of Sympathetic Innervation in the Absence of Infarction

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Regional 11C-Hydroxyephedrine Retention in Hibernating Myocardium: Chronic Inhomogeneity of Sympathetic Innervation in the Absence of Infarction Regional 11C-Hydroxyephedrine Retention in Hibernating Myocardium: Chronic Inhomogeneity of Sympathetic Innervation in the Absence of Infarction Andrew J. Luisi, Jr., MD1; Gen Suzuki, MD, PhD1; Robert deKemp, PhD2; Michael S. Haka, PhD3; Steven A. Toorongian, BS3; John M. Canty, Jr., MD1,4; and James A. Fallavollita, MD1 1Department of Medicine, SUNY at Buffalo, VA Western New York Health Care System, Buffalo, New York; 2Cardiac PET Centre, University of Ottawa Heart Institute, Ottawa, Ontario, Canada; 3Department of Nuclear Medicine, SUNY at Buffalo, Buffalo, New York; and 4Department of Physiology/Biophysics, SUNY at Buffalo, Buffalo, New York nating myocardium. Conclusion: Hibernating myocardium is We have previously shown that ex vivo counting of 131I-meta- associated with persistent reductions in regional uptake of nor- iodobenzylguanidine can identify regional reductions in sympa- epinephrine by sympathetic nerves. The inhomogeneity in sym- thetic norepinephrine uptake in pigs with hibernating myocar- pathetic innervation in viable dysfunctional myocardium is sim- dium. However, nonneuronal uptake limited relative differences ilar to that occurring after myocardial infarction and may between regions and would preclude accurate assessment with contribute to arrhythmic death in patients with ischemic cardio- conventional imaging. We therefore hypothesized that the su- myopathy. perior specificity of the positron-emitting isotope 11C-hy- Key Words: hibernation; isotopes; myocardial stunning; sym- droxyephedrine (HED) would facilitate the imaging of regional pathetic nervous system differences, and we designed this study to determine whether J Nucl Med 2005; 46:1368–1374 altered uptake of norepinephrine by sympathetic nerves in via- ble, dysfunctional myocardium can be imaged in vivo and to determine the temporal progression and stability of sympathetic dysinnervation in hibernating myocardium. Methods: Pigs (n ϭ 15) were chronically instrumented with a 1.5-mm stenosis of the Inhomogeneity in myocardial sympathetic innervation has left anterior descending coronary artery, a procedure that we been hypothesized to contribute to the development of sud- have previously shown to produce viable chronically dysfunc- tional myocardium with reduced resting flow, or hibernating den cardiac death after transmural myocardial infarction (1). myocardium, after 3 mo. Physiologic studies and HED PET were Infarction results in denervation of the scar, and interruption performed 1–5 mo later with the animals in the closed-chest of sympathetic nerves causes denervation in adjacent viable sedated state. One animal with a myocardial infarct was ana- myocardium (2,3). Subsequent reinnervation occurs slowly lyzed separately. Results: After 3 mo, anterior hypokinesis de- and is accompanied by nerve sprouting (4), which may Ϯ Ϯ Ͻ veloped (wall thickening, 32% 4% vs. 60% 4%, P 0.001), result in hyperinnervation and further exacerbate the heter- with reductions in resting flow (subendocardial flow, 0.81 Ϯ 0.11 vs. 1.20 Ϯ 0.18 mL/min/g, P Ͻ 0.05) and a critical reduction in ogeneity in sympathetic function (5). The resultant increase subendocardial flow reserve (subendocardial adenosine flow, in spatial dispersion of ventricular repolarization during 0.53 Ϯ 0.20 vs. 3.96 Ϯ 0.43 mL/min/g, P Ͻ 0.001). Extensive sympathetic activation has been hypothesized to lead to defects in HED uptake were found for hibernating myocardium, lethal ventricular arrhythmias after myocardial infarction with regional retention ϳ50% lower than that in normally per- (6), and a similar mechanism may underlie the association Ϯ Ϯ fused remote myocardium (0.035 0.002 vs. 0.066 0.002 of reduced norepinephrine-tracer uptake and cardiovascular minϪ1, P Ͻ 0.001). Relative HED uptake (left anterior descending coronary artery/remote) was lower in chronically instrumented mortality in patients with ischemic cardiomyopathy (7). animals than in control animals (n ϭ 4, P Ͻ 0.001) and animals Sympathetic nerves are exquisitely sensitive to ischemia studied 1 mo after instrumentation (n ϭ 2, P Ͻ 0.05). The and may become dysfunctional after episodes of myocardial regional reduction in sympathetic nerve function was persistent ischemia that do not result in irreversible myocyte injury and unaltered for at least 2 mo after the development of hiber- (8,9). This fact is consistent with clinical studies showing that the area of denervation is larger than that of infarction and more closely correlates with the area at risk of ischemia Received Jan. 26, 2005; revision accepted Mar. 29, 2005. For correspondence or reprints contact: James A. Fallavollita, MD, Biomed- (10). Furthermore, abnormal norepinephrine-tracer uptake ical Research Building, Room 361, Department of Medicine/Cardiology, has been described in patients without previous infarction SUNY at Buffalo, 3435 Main St., Buffalo, NY 14214. E-mail: [email protected] (11). These data suggested to us that sympathetic nerve 1368 THE JOURNAL OF NUCLEAR MEDICINE • Vol. 46 • No. 8 • August 2005 dysfunction may also contribute to the sudden death asso- ence withdrawal sample was taken from the arterial introducer ciated with hibernating myocardium in the absence of in- (17,20). Subsequently, vasodilated flow was determined during farction (12). We initiated this line of investigation using the adenosine infusion (0.9 mg/kg/min), with phenylephrine coinfused norepinephrine tracer 131I-metaiodobenzylguanidine (MIBG) to maintain arterial pressure (17). The catheters were then re- in chronically instrumented pigs with hibernating myocar- moved, and the animals were allowed to recover before the PET studies. dium (13), which have a high rate of spontaneous, arrhyth- mic sudden death (14). Although we found a significant PET Protocol regional reduction in MIBG uptake in hibernating myocar- PET was performed on 12 pigs with hibernating myocardium dium using ex vivo tissue counting, regional differences in (126 Ϯ 9 d after initial instrumentation). One of these animals was tracer uptake were limited by nonneuronal myocardial up- studied serially at 2 and 3 mo after instrumentation. Additional take and would preclude accurate imaging. Therefore, the studies were performed on 2 animals after 1 mo to assess the effects of instrumentation on uptake of norepinephrine by myo- present study was conducted with 11C-hydroxyephedrine cardial sympathetic nerves, on an animal with nontransmural in- (HED) and PET (11,15,16) to determine the feasibility of farction, and on 4 noninstrumented control animals. The pigs were imaging the time course and stability of sympathetic dys- sedated with a mixture of tiletamine hydrochloride (50 mg/mL) innervation in pigs with hibernating myocardium. Our re- and zolazepam hydrochloride (50 mg/mL) (Telazol; Wyeth Hold- sults demonstrate profound reductions in myocardial HED ings Corp.) and with xylazine (100 mg/mL) (0.022 mL/kg intra- retention in hibernating myocardium. These defects per- muscularly), with supplemental doses (0.011 mL/kg intramuscu- sisted for at least 2 mo after the development of hibernating larly) as needed. myocardium and were much greater in magnitude than HED was synthesized by direct N-methylation of metaraminol those demonstrated by ex vivo counting of MIBG (13). free base with 11C-methyl iodide in dimethyl formamide. The mixture was heated at 100°C for 5 min with semipreparative MATERIALS AND METHODS reverse-phase high-performance liquid chromatography purifica- tion (15). Scanning was performed on an ECAT 951/31-R PET All experimental procedures and protocols conformed to insti- camera (Siemens/CTI) with a 10.8-cm axial field of view and a tutional guidelines for the care and use of animals in research. resolution of ϳ5.9 mm3 in full width at half maximum. After a Initial Instrumentation 5-min transmission scan with a retractable 68Ga/68Ge rod source Studies were conducted on farm-bred pigs that were chronically had been obtained to confirm correct positioning, a 15-min trans- instrumented to produce hibernating myocardium. The initial in- mission scan was obtained to correct for attenuation. HED (dose, strumentation and experimental protocol have been published in 703 Ϯ 2 MBq [19.0 Ϯ 0.06 mCi]; nominal specific activity, 11.1 detail (17,18). Briefly, juvenile pigs (8.9 Ϯ 0.5 kg, n ϭ 15) were GBq/␮mol [300 mCi/␮mol]) was injected intravenously over 30 s instrumented with a 1.5-mm Delrin (DuPont) stenosis on the while heart rate and blood pressure were monitored noninvasively. proximal left anterior descending coronary artery (LAD). We have Imaging began at the time of tracer injection and continued for a previously shown that after 3 mo, this instrumentation results in total of 60 min, using the following image sequence: 6 ϫ 30 s, 2 ϫ viable dysfunctional myocardium with reduced resting flow, con- 60 s, 2 ϫ 150 s, 2 ϫ 300 s, 2 ϫ 600 s, and 1 ϫ 1,200 s. All animals sistent with hibernating myocardium (17,18). tolerated the imaging and recovered uneventfully. Physiologic Study Image Reconstruction Physiologic studies to document flow and function in hibernat- Emission data were corrected for attenuation and reconstructed ing myocardium were performed on animals that were in the using filtered backprojection and a Hann filter (cutoff frequency, closed-chest, propofol-sedated state (2–5 mg/kg/min intrave- 0.3 cycles per pixel). A summed HED image from 20 to 60 min nously) 118 Ϯ 9 d after initial instrumentation (n ϭ 10). A after injection was used for generation of polar maps as follows. transducer-tipped catheter (Millar
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