Radionuclide imaging of cardiac autonomic innervation

doi:10.1007/s12350-010-9239-x

Journal of Nuclear Cardiology

Volume 17, Issue 4, August 2010, Pages 655-666

https://doi.org/10.1007/s12350-010-9239-x Get rights and content

Abstract

Cardiac autonomic function plays a crucial role in health and disease, with abnormalities both reflecting the severity of the disease and contributing specifically to clinical deterioration and poor prognosis. Radiotracer analogs of the sympathetic mediator norepinephrine have been investigated extensively, and are at the brink of potential widespread clinical use. The most widely studied SPECT tracer, I-123 metaiodobenzylguanidine (¹²³I-mIBG) has consistently shown a strong, independent ability to risk stratify patients with advanced congestive heart failure. Increased global cardiac uptake appears to have a high negative predictive value in terms of cardiac events, especially death and arrhythmias, and therefore and may have a role in guiding therapy, particularly by helping to better select patients unresponsive to conventional medical therapies who would benefit from device therapies such as an ICD (implantable cardioverter defibrillator), CRT (cardiac resynchronization therapy), LVAD (left ventricular assist device), or cardiac transplantation. Cardiac autonomic imaging with SPECT and PET tracers also shows potential to assess patients following cardiac transplant, those with primary arrhythmic condition, coronary artery disease, diabetes mellitus, and during cardiotoxic chemotherapy. Radiotracer imaging of cardiac autonomic function allows visualization and quantitative measurements of underlying molecular aspects of cardiac disease, and should therefore provide a perspective that other cardiac tests cannot.

Introduction

Autonomic neuronal innervation plays a critical role in cardiac function. The heart is richly innervated with sympathetic and parasympathetic fibers that work in conjunction with circulating catecholamine mediators, such as norepinephrine (NE), to precisely regulate cardiac output at rest and during periods of increased cardiovascular demand. An impairment of cardiac autonomic function, usually the result of cardiac disease, both reflects the severity of the condition and contributes to the pathophysiologic impairment that can worsen patient outcome. As cardiac autonomic function involves molecular processes, imaging with radionuclide tracers is an ideal method of assessment.

Cardiac autonomic function is controlled by various centers in the brain that respond to incoming signals from peripheral receptors. Sympathetic efferent signals following descending pathways from the brain through the spinal cord, synapsing with pre-ganglionic fibers that leave the spinal cord at levels T1-L3, subsequently synapsing with post-ganglionic fibers that innervate both ventricles. Sympathetic nerves follow the coronary arteries in the subepicardium before penetrating the myocardium. The principle chemical mediator of sympathetic function is norepinephrine.¹^,²

Parasympathetic fibers are scarce in comparison with sympathetic. They originate in the medulla and follow the vagus nerves. In the heart they start epicardially, cross the AV groove and then penetrate the myocardium, located thereafter in the subendocardium. Parasympathetic fibers innervate the atria but are scare in the ventricle (mostly the inferior wall), and also modulate SA and AV nodal function. The major chemical mediator of parasympathetic function is acetylcholine.

Most published literature and current clinical applicability of autonomic radionuclide imaging is of the sympathetic system, with parasympathetic imaging studies limited mostly to animals. Therefore, the following discussion will deal predominantly with cardiac sympathetic imaging.

Section snippets

Radionuclide Tracers

Cardiac sympathetic innervation imaging currently focuses on the synaptic junction, illustrated in Figure 1.³ Most radiotracers that have been developed image pre-synaptic anatomy and function, but newer tracers that bind to post-synaptic α and β receptors are also being designed and investigated.

Norepinephrine (NE) is produced in the presynaptic sympathetic nerve terminal through multiple biochemical processes starting with tyrosine, and ultimately stored at high concentrations in presynaptic

Imaging Methods and Interpretation

Intravenous injection of ¹²³I-mIBG is performed at rest, and needs only minimal preparation. Medications that might interfere with catecholamine uptake, such as various antidepressants, antipsychotics, and some calcium channel blockers, should be held for 24 hours before tracer injection and imaging. There are differences of opinion regarding the need for administration of thyroid-blocking agents before ¹²³I-mIBG administration. Historically such blockade has been undertaken to shield the

Neuronal Imaging in Congestive Heart Failure

Congestive heart failure (CHF) is a worsening epidemic in developed countries due in large part to a progressively aging population and to better survival from acute cardiac events that leave patients with damaged hearts. In the United States close to 5 million people have CHF, with 550,000 new cases each year. Mortality can reach 50% annually, with CHF being a major underlying or contributing cause of death in close to 300,000 people per year. CHF is an expensive condition with more Medicare

Potential Role of ¹²³I-mIBG in Guiding Therapy for CHF

While the use of cardiac adrenergic imaging to risk stratify patients may have value in itself, the potential to more effectively guide specific therapies would provide greater clinical utility. There are numerous reports demonstrating that ¹²³I-mIBG imaging effectively monitors the effects of conventional CHF medical therapies. As one might expect, ¹²³I-mIBG images frequently improve after institution of β-blocker therapy, associated in some studies with decreased ventricular volumes, improved

¹²³I-mIBG Imaging and Ventricular Arrhythmias

A major cause of death in patients with advanced heart failure is ventricular arrhythmia-induced sudden cardiac death (SCD).⁵⁷ While in some cases the terminal arrhythmia is the natural result of end-stage irreversible pump dysfunction, in other cases a patient may otherwise be doing relatively well only to be struck down by SCD. For the latter reason, based on trials such as SCD-HEFT, it is a Class IA indication that patients with LVEF ≤ 35% receive a prophylactic implantable cardioverter

Primary Arrhythmic Disease

In addition to having potential clinical utility in CHF-associated ventricular arrhythmias, imaging with ¹²³I-mIBG or similar tracers has shown cardiac abnormalities in patients with primary arrhythmic conditions. Mitrani and colleagues saw regional sympathetic denervation in 55% of patients who presented with VT but had structurally normal hearts compared with none in controls.⁷⁵ Gill and colleagues found asymmetrical uptake of ¹²³I-mIBG in about half of the patients they studied who had VT

Cardiac Transplantation

During cardiac transplantation, postganglionic sympathetic fibers of the donor heart are interrupted, resulting in complete sympathetic denervation of the transplanted heart. The new heart thus has an impaired response to the demands of exercise. Over time, though, at least some sympathetic reinnervation occurs.79, 80, 81 Bengel and colleagues used ¹¹C-HED imaging to demonstrate progressive post-transplant cardiac reinnervation, with a follow-up study showing a correlation with an enhanced

¹²³I-mIBG Imaging in Ischemic Heart Disease

Sympathetic nerve trunks course along the coronary arterial pathways before penetrating the myocardium. Myocardial ischemia/infarction disrupts sympathetic transmission, in which case myocardium distal to and beyond the site of injury but not otherwise involved in the ischemic process may be affected. In addition cardiac sympathetic nervous tissue is more sensitive to ischemia than myocytes, and takes longer to recover. The result can be perfused and viable, but denervated myocardium, with such

¹²³I-mIBG Imaging and Diabetes Mellitus

Diabetes is a systemic, multi-organ disease, with morbidity and mortality increased by the presence of autonomic neuropathy. While various noninvasive tests help to detect the presence of diabetic-induced neuropathy, they predominantly assess parasympathetic function. Cardiac imaging assessment of sympathetic function may provide a unique approach to assess neuropathy. Stevens and colleagues found abnormalities of ¹¹C-HED retention in 40% of autonomic neuropathy-free diabetic patients, first

¹²³I-mIBG Imaging and Chemotherapy

Given the enhanced sensitivity of sympathetic nerves to myocardial insults, neuronal imaging has been investigated as a potential method of assessing cardiac damage from chemotherapy. In rat studies, Wakasugi and colleagues showed that doxorubicin administration resulted in a decrease in cardiac uptake of ¹²⁵I-mIBG, preceding a decrease in LVEF.⁸⁸ In humans, Olmos and colleagues reported decreased cardiac uptake of ¹²³I-mIBG as the cumulative dose of doxorubicin increased, followed by

Postsynaptic Sympathetic Imaging

Cardiac postsynaptic receptors transmit sympathetic signal to the myocardial tissue, regulating chronotropic, dromotropic, and inotropic cardiac effects, and are good targets for imaging. At this time only a few radiotracers have been synthesized for it, the main problem being the difficulty of finding a compound that is easily made and has sufficient specificity.⁹¹ Some clinical work has been done with ¹¹CCGP12177, a nonselective, hydrophilic β-receptor binding agent that produces good-quality

Imaging of the Cardiac Parasympathetic System

Abnormalities of parasympathetic activity also contribute to cardiac pathophysiology. Parasympathetic innervation and activation can induce and maintain atrial fibrillation, whereas ablation can induce parasympathetic denervation and improve clinical outcome.⁹³^,⁹⁴ Due to the lack of sufficient experience and data, imaging of cardiac parasympathetic system has been limited. There is a low density of cholinergic neurons in the heart, as well as difficulty in tracer design because of rapid

Conclusions

Disruption of the cardiac neuronal system may occur as a result of cardiac disease and/or itself may be the cause of cardiac problems. Cardiac neuronal abnormalities occur in a variety of cardiac disease states and patients with cardiac neuronal abnormalities are at increased risk, including a higher potential for sudden, arrhythmic death. Thus, the ability to image cardiac neuronal system with radiotracers should be a powerful tool to assess and risk-stratify patients, and to guide the

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A insuficiência cardíaca é um problema à escala global, com uma prevalência estimada nos países desenvolvidos de 2%. Apresenta uma mortalidade elevada, sendo a morte súbita cardíaca a principal causa. A disfunção do sistema nervoso autónomo, nomeadamente a hiperatividade simpática, que acompanha a insuficiência cardíaca crónica, relaciona-se com a remodelação progressiva do miocárdio, o declínio da função ventricular esquerda e o agravamento dos sintomas, participando no desenvolvimento de arritmias ventriculares e morte súbita.
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Metaiodobenzylguanidine (MIBG) is a false neurotransmitter noradrenaline analogue that is taken up by the ‘uptake 1’ transporter mechanism in the cell membrane of presynaptic adrenergic neurons and accumulates in catecholamine storage vesicles. Since it is practically unmetabolized, it can be labeled with a radioisotope (iodine-123) in scintigraphic exams to noninvasively assess the functional status of the sympathetic innervation of organs with a significant adrenergic component, including the heart. Studies of its application in nuclear cardiology appear to confirm its value in the assessment of conditions such as coronary artery disease, heart failure, arrhythmias and sudden death.
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Review ArticleRadionuclide imaging of cardiac autonomic innervation

Abstract

Introduction

Section snippets

Radionuclide Tracers

Imaging Methods and Interpretation

Neuronal Imaging in Congestive Heart Failure

Potential Role of 123I-mIBG in Guiding Therapy for CHF

123I-mIBG Imaging and Ventricular Arrhythmias

Primary Arrhythmic Disease

Cardiac Transplantation

123I-mIBG Imaging in Ischemic Heart Disease

123I-mIBG Imaging and Diabetes Mellitus

123I-mIBG Imaging and Chemotherapy

Postsynaptic Sympathetic Imaging

Imaging of the Cardiac Parasympathetic System

Conclusions

Cardiol Clin

J Nucl Cardiol

J Nucl Cardiol

J Nucl Cardiol

J Nucl Cardiol

J Am Coll Cardiol

J Nucl Cardiol

J Am Coll Cardiol

Am Heart J

J Nucl Cardiol

J Am Coll Cardiol

J Nucl Cardiol

Am J Cardiol

J Cardiac Fail

J Nucl Cardiol

J Nucl Cardiol

J Nucl Cardiol

Am Heart J

J Nucl Cardiol

J Nucl Cardiol

J Am Coll Cardiol Img

J Am Coll Cardiol

J Am Coll Cardiol

J Am Coll Cardiol

J Am Coll Cardiol

J Am Coll Cardiol

Am J Cardiol

J Nucl Cardiol

J Am Coll Cardiol

J Am Coll Cardiol

Am Heart J

J Nucl Cardiol

Eur J Cancer

J Am Coll Cardiol

J Am Coll Cardiol

Cardiac neurotransmission imaging

J Nucl Med

Autonomic modulation of cardiac arrhythmias

Cardiac electrophysiology: From cell to bedside

Autonomic aspects of arrhythmogenesis: The enduring and the new

Curr Opin Cardiol

Radiolabelled meta-iodobenzylguanidine pharmacology: Pharmacology and clinical studies

Am J Physiol Imaging

Metaiodobenzylguanidine scintigraphy of the heart. What have we learned clinically?

Eur J Nucl Med

Myocardial imaging in man with I-123 Meta-iodobenzylguanidine

J Nucl Med

Myocardial imaging with a radioiodinated norepinephrine storage analog

J Nucl Med

Regional 11C-hydroxyephedrine retention in hibernating myocardium: Chronic inhomogeneity of sympathetic innervation in the absence of infarction

J Nucl Med

Heart failure imaging in the rat with LMI1195: A new PET cardiac neuronal imaging agent

Circulation

LMI1195: A new 18F benzylguanidine analog for PET cardiac sympathetic neuronal imaging

J Am Coll Cardiol

Prognostic significance of cardiac 123I metaiodobenzylguanidine imaging for mortality and morbidity in patients with chronic heart failure: A prospective study

Heart

MIBG imaging

J Nucl Cardiol

Review Article
Radionuclide imaging of cardiac autonomic innervation

Potential Role of ¹²³I-mIBG in Guiding Therapy for CHF

¹²³I-mIBG Imaging and Ventricular Arrhythmias

¹²³I-mIBG Imaging in Ischemic Heart Disease

¹²³I-mIBG Imaging and Diabetes Mellitus

¹²³I-mIBG Imaging and Chemotherapy