Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Clinical Autonomic Research
Published in: Clinical Autonomic Research 4/2018

01-08-2018 | Review

Roles of cardiac sympathetic neuroimaging in autonomic medicine

Authors: David S. Goldstein, William P. Cheshire Jr.

Published in: Clinical Autonomic Research | Issue 4/2018

Login to get access

Abstract

Sympathetic neuroimaging is based on the injection of compounds that either radiolabel sites of the cell membrane norepinephrine transporter (NET) or that are taken up into sympathetic nerves via the NET and radiolabel intra-neuronal catecholamine storage sites. Detection of the radioactivity is by planar or tomographic radionuclide imaging. The heart stands out among body organs in terms of the intensity of radiolabeling of sympathetic nerves, and virtually all of sympathetic neuroimaging focuses on the left ventricular myocardium. The most common cardiac sympathetic neuroimaging method worldwide is 123I-metaiodobenzylguanidine (123I-MIBG) scanning. 123I-MIBG scanning is used routinely in Europe and East Asia in the diagnostic evaluation of neurogenic orthostatic hypotension (nOH), to distinguish Lewy body diseases (e.g., Parkinson disease with orthostatic hypotension (OH), pure autonomic failure) from non-Lewy body diseases (e.g., multiple system atrophy) and to distinguish dementia with Lewy bodies from Alzheimer’s disease. In the USA, 123I-MIBG scanning has been approved by the Food and Drug Administration for the evaluation of pheochromocytoma and some forms of heart failure—but not for the above-mentioned differential diagnoses. Positron emission tomographic methods based on imaging agents such as 18F-dopamine are categorized as research tools, despite more than a quarter century of clinical experience with these modalities. Considering that 123I-MIBG scanning is available at most academic medical centers in the USA, cardiac sympathetic neuroimaging by this methodology merits consideration as an autonomic test, especially in patients with nOH.
Literature
1.
Abbasi M, Ghalandari N, Farzanefar S, Aghamollaii V, Ahmadi M, Ganji M, Afarideh M, Loloee S, Naseri M, Tafakhori A (2017) Potential diagnostic value of (131)I-MIBG myocardial scintigraphy in discrimination between Alzheimer disease and dementia with Lewy bodies. Clin Neurol Neurosurg 163:163–166PubMedCrossRef
2.
Agostini D, Babatasi G, Manrique A, Saloux E, Grollier G, Potier JC, Bouvard G (1998) Impairment of cardiac neuronal function in acute myocarditis: iodine-123-MIBG scintigraphy study. J Nucl Med 39:1841–1844PubMed
3.
Agostini D, Belin A, Amar MH, Darlas Y, Hamon M, Grollier G, Potier JC, Bouvard G (2000) Improvement of cardiac neuronal function after carvedilol treatment in dilated cardiomyopathy: a 123I-MIBG scintigraphic study. J Nucl Med 41:845–851PubMed
4.
Akashi YJ, Goldstein DS, Barbaro G, Ueyama T (2008) Takotsubo cardiomyopathy: a new form of acute, reversible heart failure. Circulation 118:2754–2762PubMedPubMedCentralCrossRef
5.
Akashi YJ, Nakazawa K, Sakakibara M, Miyake F, Musha H, Sasaka K (2004) 123I-MIBG myocardial scintigraphy in patients with “takotsubo” cardiomyopathy. J Nucl Med 45:1121–1127PubMed
6.
Akashi YJ, Nakazawa K, Sakakibara M, Miyake F, Sasaka K (2002) Reversible left ventricular dysfunction “takotsubo” cardiomyopathy related to catecholamine cardiotoxicity. J Electrocardiol 35:351–356PubMedCrossRef
7.
Algalarrondo V, Antonini T, Theaudin M, Chemla D, Benmalek A, Lacroix C, Castaing D, Cauquil C, Dinanian S, Eliahou L, Samuel D, Adams D, Le Guludec D, Slama MS, Rouzet F (2016) Cardiac dysautonomia predicts long-term survival in hereditary transthyretin amyloidosis after liver transplantation. JACC Cardiovasc Imaging 9:1432–1441PubMedCrossRef
8.
Amino T, Orimo S, Takahashi A, Uchihara T, Mizusawa H (2005) Profound cardiac sympathetic denervation occurs in Parkinson disease. Brain Pathol 15:29–34PubMedCrossRef
9.
Berardelli A, Wenning GK, Antonini A, Berg D, Bloem BR, Bonifati V, Brooks D, Burn DJ, Colosimo C, Fanciulli A, Ferreira J, Gasser T, Grandas F, Kanovsky P, Kostic V, Kulisevsky J, Oertel W, Poewe W, Reese JP, Relja M, Ruzicka E, Schrag A, Seppi K, Taba P, Vidailhet M (2013) EFNS/MDS-ES/ENS recommendations for the diagnosis of Parkinson’s disease. Eur J Neurol 20:16–34PubMedCrossRef
10.
Boogers MJ, Borleffs CJ, Henneman MM, van Bommel RJ, van Ramshorst J, Boersma E, Dibbets-Schneider P, Stokkel MP, van der Wall EE, Schalij MJ, Bax JJ (2010) Cardiac sympathetic denervation assessed with 123-iodine metaiodobenzylguanidine imaging predicts ventricular arrhythmias in implantable cardioverter-defibrillator patients. J Am Coll Cardiol 55:2769–2777PubMedCrossRef
11.
12.
Braune S (2001) The role of cardiac metaiodobenzylguanidine uptake in the differential diagnosis of parkinsonian syndromes. Clin Auton Res 11:351–355PubMedCrossRef
13.
Braune S, Reinhardt M, Schnitzer R, Riedel A, Lucking CH (1999) Cardiac uptake of [123I]MIBG separates Parkinson’s disease from multiple system atrophy. Neurology 53:1020–1025PubMedCrossRef
14.
Burgdorf C, Kurowski V, Bonnemeier H, Schunkert H, Radke PW (2008) Long-term prognosis of the transient left ventricular dysfunction syndrome (Tako-Tsubo cardiomyopathy): focus on malignancies. Eur J Heart Fail 10:1015–1019PubMedCrossRef
15.
Chizzola PR, Goncalves de Freitas HF, Marinho NV, Mansur JA, Meneghetti JC, Bocchi EA (2006) The effect of beta-adrenergic receptor antagonism in cardiac sympathetic neuronal remodeling in patients with heart failure. Int J Cardiol 106:29–34PubMedCrossRef
16.
Christensen TE, Bang LE, Holmvang L, Skovgaard DC, Oturai DB, Soholm H, Thomsen JH, Andersson HB, Ghotbi AA, Ihlemann N, Kjaer A, Hasbak P (2016) (123)I-MIBG scintigraphy in the subacute state of takotsubo cardiomyopathy. JACC Cardiovasc Imaging 9:982–990PubMedCrossRef
17.
Coates G, Chirakal R, Fallen EL, Firnau G, Garnett ES, Kamath MV, Scheffel A, Nahmias C (1996) Regional distribution and kinetics of [18F]6-flurodopamine as a measure of cardiac sympathetic activity in humans. Heart 75:29–34PubMedPubMedCentralCrossRef
18.
Cook GA, Sullivan P, Holmes C, Goldstein DS (2014) Cardiac sympathetic denervation without Lewy bodies in a case of multiple system atrophy. Parkinsonism Relat Disord 20:926–928PubMedPubMedCentralCrossRef
19.
Courbon F, Brefel-Courbon C, Thalamas C, Alibelli MJ, Berry I, Montastruc JL, Rascol O, Senard JM (2003) Cardiac MIBG scintigraphy is a sensitive tool for detecting cardiac sympathetic denervation in Parkinson’s disease. Mov Disord 18:890–897PubMedCrossRef
20.
de Milliano PA, de Groot AC, Tijssen JG, van Eck-Smit BL, Van Zwieten PA, Lie KI (2002) Beneficial effects of metoprolol on myocardial sympathetic function: evidence from a randomized, placebo-controlled study in patients with congestive heart failure. Am Heart J 144:E3PubMedCrossRef
21.
Didangelos T, Moralidis E, Karlafti E, Tziomalos K, Margaritidis C, Kontoninas Z, Stergiou I, Boulbou M, Papagianni M, Papanastasiou E, Hatzitolios AI (2018) A comparative assessment of cardiovascular autonomic reflex testing and cardiac (123)I-metaiodobenzylguanidine imaging in patients with type 1 diabetes mellitus without complications or cardiovascular risk factors. Int J Endocrinol 2018:5607208PubMedPubMedCentralCrossRef
22.
Ding YS, Fowler JS, Dewey SL, Logan J, Schlyer DJ, Gatley SJ, Volkow ND, King PT, Wolf AP (1993) Comparison of high specific activity (-) and (+)-6-[18F]fluoronorepinephrine and 6-[18F]fluorodopamine in baboons: heart uptake, metabolism and the effect of desipramine. J Nucl Med 34:619–629PubMed
23.
Ding YS, Fowler JS, Gatley SJ, Dewey SL, Wolf AP, Schlyer DJ (1991) Synthesis of high specific activity 6-[18F]fluorodopamine for positron emission tomography studies of sympathetic nervous tissue. J Med Chem 34:861–863PubMedCrossRef
24.
Ding YS, Fowler JS, Gatley SJ, Logan J, Volkow ND, Shea C (1995) Mechanistic positron emission tomography studies of 6-[18F]fluorodopamine in living baboon heart: selective imaging and control of radiotracer metabolism using the deuterium isotope effect. J Neurochem 65:682–690PubMedCrossRef
25.
Donadio V, Cortelli P, Elam M, Di Stasi V, Montagna P, Holmberg B, Giannoccaro MP, Bugiardini E, Avoni P, Baruzzi A, Liguori R (2010) Autonomic innervation in multiple system atrophy and pure autonomic failure. J Neurol Neurosurg Psychiatry 81:1327–1335PubMedCrossRef
26.
Donadio V, Incensi A, Piccinini C, Cortelli P, Giannoccaro MP, Baruzzi A, Liguori R (2016) Skin nerve misfolded alpha-synuclein in pure autonomic failure and Parkinson disease. Ann Neurol 79:306–316PubMedCrossRef
27.
Druschky A, Hilz MJ, Platsch G, Radespiel-Troger M, Druschky K, Kuwert T, Neundorfer B (2000) Differentiation of Parkinson’s disease and multiple system atrophy in early disease stages by means of I-123-MIBG-SPECT. J Neurol Sci 175:3–12PubMedCrossRef
28.
Eisenhofer G, Friberg P, Rundqvist B, Quyyumi AA, Lambert G, Kaye DM, Kopin IJ, Goldstein DS, Esler MD (1996) Cardiac sympathetic nerve function in congestive heart failure. Circulation 93:1667–1676PubMedCrossRef
29.
Eldadah BA, Pacak K, Eisenhofer G, Holmes C, Kopin IJ, Goldstein DS (2004) Cardiac uptake-1 inhibition by high circulating norepinephrine levels in patients with pheochromocytoma. Hypertension 43:1227–1232PubMedCrossRef
30.
Fujishiro H, Nakamura S, Kitazawa M, Sato K, Iseki E (2012) Early detection of dementia with Lewy bodies in patients with amnestic mild cognitive impairment using 123I-MIBG cardiac scintigraphy. J Neurol Sci 315:115–119PubMedCrossRef
31.
Gagnon N, Mansour S, Bitton Y, Bourdeau I (2017) Takotsubo-like cardiomyopathy in a large cohort of patients with pheochromocytoma and paraganglioma. Endocr Pract 23:1178–1192PubMedCrossRef
32.
Gerson MC, McGuire N, Wagoner LE (2003) Sympathetic nervous system function as measured by I-123 metaiodobenzylguanidine predicts transplant-free survival in heart failure patients with idiopathic dilated cardiomyopathy. J Card Fail 9:384–391PubMedCrossRef
33.
Giannoccaro MP, Donadio V, Incensi A, Pizza F, Cason E, Di Stasi V, Martinelli P, Scaglione C, Capellari S, Treglia G, Liguori R (2015) Skin biopsy and I-123 MIBG scintigraphy findings in idiopathic Parkinson’s disease and parkinsonism: a comparative study. Mov Disord 30:986–989PubMedCrossRef
34.
Giordano A, Calcagni ML, Verrillo A, Pellegrinotti M, Frontoni S, Spallone V, Gambardella S (2000) Assessment of sympathetic innervation of the heart in diabetes mellitus using 123I-MIBG. Diabetes Nutr Metab 13:350–355PubMed
35.
Goldstein DS (2016) Cardiac dysautonomia and survival in hereditary transthyretin amyloidosis. JACC Cardiovasc Imaging 9:1442–1445PubMedCrossRef
36.
Goldstein DS, Chang PC, Eisenhofer G, Miletich R, Finn R, Bacher J, Kirk KL, Bacharach S, Kopin IJ (1990) Positron emission tomographic imaging of cardiac sympathetic innervation and function. Circulation 81:1606–1621PubMedCrossRef
37.
Goldstein DS, Cheshire WP (2018) Roles of catechol neurochemistry in autonomic function testing. Clin Auton Res 28(3):273–288
38.
Goldstein DS, Eisenhofer G, Dunn BB, Armando I, Lenders J, Grossman E, Holmes C, Kirk KL, Bacharach S, Adams R et al (1993) Positron emission tomographic imaging of cardiac sympathetic innervation using 6-[18F]fluorodopamine: initial findings in humans. J Am Coll Cardiol 22:1961–1971PubMedCrossRef
39.
Goldstein DS, Grossman E, Tamrat M, Chang PC, Eisenhofer G, Bacher J, Kirk KL, Bacharach S, Kopin IJ (1991) Positron emission imaging of cardiac sympathetic innervation and function using 18F-6-fluorodopamine: effects of chemical sympathectomy by 6-hydroxydopamine. J Hypertens 9:417–423PubMedCrossRef
40.
Goldstein DS, Holmes C, Bentho O, Sato T, Moak J, Sharabi Y, Imrich R, Conant S, Eldadah BA (2008) Biomarkers to detect central dopamine deficiency and distinguish Parkinson disease from multiple system atrophy. Parkinsonism Relat Disord 14:600–607PubMedPubMedCentralCrossRef
41.
Goldstein DS, Holmes C, Kopin IJ, Sharabi Y (2011) Intra-neuronal vesicular uptake of catecholamines is decreased in patients with Lewy body diseases. J Clin Investig 121:3320–3330PubMedCrossRef
42.
Goldstein DS, Holmes C, Li ST, Bruce S, Metman LV, Cannon RO 3rd (2000) Cardiac sympathetic denervation in Parkinson disease. Ann Intern Med 133:338–347PubMedCrossRef
43.
Goldstein DS, Holmes C, Lopez GJ, Wu T, Sharabi Y (2018) Cardiac sympathetic denervation predicts PD in at-risk individuals. Parkinsonism Relat Disord 52:90–93
44.
Goldstein DS, Holmes C, Sharabi Y, Brentzel S, Eisenhofer G (2003) Plasma levels of catechols and metanephrines in neurogenic orthostatic hypotension. Neurology 60:1327–1332PubMedCrossRef
45.
Goldstein DS, Orimo S (2009) Cardiac sympathetic neuroimaging: summary of the first international symposium. Clin Auton Res 19:133–136CrossRef
46.
47.
48.
Haensch CA, Lerch H, Jorg J, Isenmann S (2009) Cardiac denervation occurs independent of orthostatic hypotension and impaired heart rate variability in Parkinson’s disease. Parkinsonism Relat Disord 15:134–137PubMedCrossRef
49.
Hakusui S, Yasuda T, Yanagi T, Tohyama J, Hasegawa Y, Koike Y, Hirayama M, Takahashi A (1994) A radiological analysis of heart sympathetic functions with meta-[123I]iodobenzylguanidine in neurological patients with autonomic failure. J Auton Nerv Syst 49:81–84PubMedCrossRef
50.
Hanyu H, Shimizu S, Hirao K, Sakurai H, Iwamoto T, Chikamori T, Hida S, Yamashina A, Koizumi K, Abe K (2006) The role of 123I-metaiodobenzylguanidine myocardial scintigraphy in the diagnosis of Lewy body disease in patients with dementia in a memory clinic. Dement Geriatr Cogn Disord 22:379–384PubMedCrossRef
51.
Imamura Y, Ando H, Mitsuoka W, Egashira S, Masaki H, Ashihara T, Fukuyama T (1995) Iodine-123 metaiodobenzylguanidine images reflect intense myocardial adrenergic nervous activity in congestive heart failure independent of underlying cause. J Am Coll Cardiol 26:1594–1599PubMedCrossRef
52.
Imperato-McGinley J, Gautier T, Ehlers K, Zullo MA, Goldstein DS, Vaughan ED Jr (1987) Reversibility of catecholamine-induced dilated cardiomyopathy in a child with a pheochromocytoma. N Engl J Med 316:793–797PubMedCrossRef
53.
Imrich R, Eldadah BA, Bentho O, Pechnik S, Sharabi Y, Holmes C, Grossman E, Goldstein DS (2009) Functional effects of cardiac sympathetic denervation in neurogenic orthostatic hypotension. Parkinsonism Relat Disord 15:122–127PubMedCrossRef
54.
Ito K, Sugihara H, Kinoshita N, Azuma A, Matsubara H (2005) Assessment of Takotsubo cardiomyopathy (transient left ventricular apical ballooning) using 99mTc-tetrofosmin, 123I-BMIPP, 123I-MIBG and 99mTc-PYP myocardial SPECT. Ann Nucl Med 19:435–445PubMedCrossRef
55.
Iversen LL (1963) The uptake of noradrenaline by the isolated perfused rat heart. Br J Pharmacol 21:523–537
56.
Izumi C, Himura Y, Konishi T (1995) Abnormal cardiac sympathetic nerve function in a patient with pheochromocytoma. An analysis using 123I metaiodobenzylguanidine scintigraphy. Int J Cardiol 50:189–192PubMedCrossRef
57.
Jacobson AF, Senior R, Cerqueira MD, Wong ND, Thomas GS, Lopez VA, Agostini D, Weiland F, Chandna H, Narula J (2010) Myocardial iodine-123 meta-iodobenzylguanidine imaging and cardiac events in heart failure. Results of the prospective ADMIRE-HF (AdreView Myocardial Imaging for Risk Evaluation in Heart Failure) study. J Am Coll Cardiol 55:2212–2221PubMedCrossRef
58.
Kakuchi H, Sasaki T, Ishida Y, Komamura K, Miyatake K (1999) Clinical usefulness of 123I meta-iodobenzylguanidine imaging in predicting the effectiveness of beta blockers for patients with idiopathic dilated cardiomyopathy before and soon after treatment. Heart 81:148–152PubMedPubMedCentralCrossRef
59.
Kasama S, Toyama T, Kumakura H, Takayama Y, Ichikawa S, Suzuki T, Kurabayashi M (2005) Effects of candesartan on cardiac sympathetic nerve activity in patients with congestive heart failure and preserved left ventricular ejection fraction. J Am Coll Cardiol 45:661–667PubMedCrossRef
60.
Kasama S, Toyama T, Sumino H, Nakazawa M, Matsumoto N, Sato Y, Kumakura H, Takayama Y, Ichikawa S, Suzuki T, Kurabayashi M (2008) Prognostic value of serial cardiac 123I-MIBG imaging in patients with stabilized chronic heart failure and reduced left ventricular ejection fraction. J Nucl Med 49:907–914PubMedCrossRef
61.
Kashihara K, Ohno M, Kawada S, Okumura Y (2006) Reduced cardiac uptake and enhanced washout of 123I-MIBG in pure autonomic failure occurs conjointly with Parkinson’s disease and dementia with Lewy bodies. J Nucl Med 47:1099–1101PubMed
62.
Kim JS, Park HE, Oh YS, Lee SH, Park JW, Son BC, Lee KS (2016) Orthostatic hypotension and cardiac sympathetic denervation in Parkinson disease patients with REM sleep behavioral disorder. J Neurol Sci 362:59–63PubMedCrossRef
63.
Kim JS, Park HE, Oh YS, Song IU, Yang DW, Park JW, Lee KS (2015) (123)I-MIBG myocardial scintigraphy and neurocirculatory abnormalities in patients with dementia with Lewy bodies and Alzheimer’s disease. J Neurol Sci 357:173–177PubMedCrossRef
64.
Kim JS, Park HE, Park IS, Oh YS, Ryu DW, Song IU, Jung YA, Yoo IR, Choi HS, Lee PH, Lee KS (2017) Normal ‘heart’ in Parkinson’s disease: is this a distinct clinical phenotype? Eur J Neurol 24:349–356PubMedCrossRef
65.
Kioka H, Yamada T, Mine T, Morita T, Tsukamoto Y, Tamaki S, Masuda M, Okuda K, Hori M, Fukunami M (2007) Prediction of sudden death in patients with mild-to-moderate chronic heart failure by using cardiac iodine-123 metaiodobenzylguanidine imaging. Heart 93:1213–1218PubMedPubMedCentralCrossRef
66.
Kobayashi S, Tateno M, Morii H, Utsumi K, Saito T (2009) Decreased cardiac MIBG uptake, its correlation with clinical symptoms in dementia with Lewy bodies. Psychiatry Res 174:76–80PubMedCrossRef
67.
Kobayashi Y, Kobayashi Y, Hirohata A (2014) Pheochromocytoma found in Takotsubo cardiomyopathy patients. J. Invasive Cardiol 26:E76–E77PubMed
68.
Koutelou M, Katsikis A, Flevari P, Theodorakis G, Livanis E, Georgiadis M, Voudris V, Kremastinos D (2009) Predictive value of cardiac autonomic indexes and MIBG washout in ICD recipients with mild to moderate heart failure. Ann Nucl Med 23:677–684PubMedCrossRef
69.
Kurata C, Shouda S, Mikami T, Uehara A, Ishikawa K, Tawarahara K, Nakano T, Matoh F, Takeuchi K (1998) Metaiodobenzylguanidine and heart rate variability in heart failure. Jpn Circ J 62:770–772PubMedCrossRef
70.
Li ST, Dendi R, Holmes C, Goldstein DS (2002) Progressive loss of cardiac sympathetic innervation in Parkinson’s disease. Ann Neurol 52:220–223PubMedCrossRef
71.
Lynn MD, Shapiro B, Sisson JC, Beierwaltes WH, Meyers LJ, Ackerman R, Mangner TJ (1985) Pheochromocytoma and the normal adrenal medulla: improved visualization with I-123 MIBG scintigraphy. Radiology 155:789–792PubMedCrossRef
72.
Manabe Y, Inui Y, Toyama H, Kosaka K (2017) 123I-metaiodobenzylguanidine myocardial scintigraphy with early images alone is useful for the differential diagnosis of dementia with Lewy bodies. Psychiatry Res 261:75–79CrossRef
73.
Mantysaari M, Kuikka J, Mustonen J, Tahvanainen K, Vanninen E, Lansimies E, Uusitupa M (1996) Measurement of myocardial accumulation of 123I-metaiodobenzylguanidine for studying cardiac autonomic neuropathy in diabetes mellitus. Clin Auton Res 6:163–169PubMedCrossRef
74.
Maser RE, Mitchell BD, Vinik AI, Freeman R (2003) The association between cardiovascular autonomic neuropathy and mortality in individuals with diabetes: a meta-analysis. Diabetes Care 26:1895–1901PubMedCrossRef
75.
Matsui H, Nishinaka K, Oda M, Komatsu K, Kubori T, Udaka F (2006) Does cardiac metaiodobenzylguanidine (MIBG) uptake in Parkinson’s disease correlate with major autonomic symptoms? Parkinsonism Relat Disord 12:284–288PubMedCrossRef
76.
Matsui H, Udaka F, Oda M, Kubori T, Nishinaka K, Kameyama M (2005) Metaiodobenzylguanidine (MIBG) scintigraphy at various parts of the body in Parkinson’s disease and multiple system atrophy. Auton Neurosci 119:56–60PubMedCrossRef
77.
Matsui T, Tsutamoto T, Maeda K, Kusukawa J, Kinoshita M (2002) Prognostic value of repeated 123I-metaiodobenzylguanidine imaging in patients with dilated cardiomyopathy with congestive heart failure before and after optimized treatments—comparison with neurohumoral factors. Circ J 66:537–543PubMedCrossRef
78.
Maunoury C, Agostini D, Acar P, Antonietti T, Sidi D, Bouvard G, Kachaner J, Barritault L (2000) Impairment of cardiac neuronal function in childhood dilated cardiomyopathy: an 123I-MIBG scintigraphic study. J Nucl Med 41:400–404PubMed
79.
McKeith IG, Boeve BF, Dickson DW, Halliday G, Taylor JP, Weintraub D, Aarsland D, Galvin J, Attems J, Ballard CG, Bayston A, Beach TG, Blanc F, Bohnen N, Bonanni L, Bras J, Brundin P, Burn D, Chen-Plotkin A, Duda JE, El-Agnaf O, Feldman H, Ferman TJ, Ffytche D, Fujishiro H, Galasko D, Goldman JG, Gomperts SN, Graff-Radford NR, Honig LS, Iranzo A, Kantarci K, Kaufer D, Kukull W, Lee VMY, Leverenz JB, Lewis S, Lippa C, Lunde A, Masellis M, Masliah E, McLean P, Mollenhauer B, Montine TJ, Moreno E, Mori E, Murray M, O’Brien JT, Orimo S, Postuma RB, Ramaswamy S, Ross OA, Salmon DP, Singleton A, Taylor A, Thomas A, Tiraboschi P, Toledo JB, Trojanowski JQ, Tsuang D, Walker Z, Yamada M, Kosaka K (2017) Diagnosis and management of dementia with Lewy bodies: fourth consensus report of the DLB Consortium. Neurology 89:88–100PubMedPubMedCentralCrossRef
80.
Meredith IT, Eisenhofer G, Lambert GW, Dewar EM, Jennings GL, Esler MD (1993) Cardiac sympathetic nervous activity in congestive heart failure. Evidence for increased neuronal norepinephrine release and preserved neuronal uptake. Circulation 88:136–145PubMedCrossRef
81.
Merlet P, Benvenuti C, Moyse D, Pouillart F, Dubois-Rande JL, Duval AM, Loisance D, Castaigne A, Syrota A (1999) Prognostic value of MIBG imaging in idiopathic dilated cardiomyopathy. J Nucl Med 40:917–923PubMed
82.
Nakajima K, Okuda K, Yoshimura M, Matsuo S, Wakabayashi H, Imanishi Y, Kinuya S (2014) Multicenter cross-calibration of I-123 metaiodobenzylguanidine heart-to-mediastinum ratios to overcome camera-collimator variations. J Nucl Cardiol 21:970–978PubMedPubMedCentralCrossRef
83.
Nakajima K, Yoshita M, Matsuo S, Taki J, Kinuya S (2008) Iodine-123-MIBG sympathetic imaging in Lewy-body diseases and related movement disorders. Q J Nucl Med Mol Imaging 52:378–387PubMed
84.
Nakamura T, Hirayama M, Hara T, Mizutani Y, Suzuki J, Watanabe H, Sobue G (2014) Role of cardiac sympathetic nerves in preventing orthostatic hypotension in Parkinson’s disease. Parkinsonism Relat Disord 20:409–414PubMedCrossRef
85.
Niimi Y, Ito S, Murate K, Hirota S, Hikichi C, Ishikawa T, Maeda T, Nagao R, Shima S, Mizutani Y, Ueda A, Mutoh T (2017) Usefulness of combining (123)I-FP-CIT-SPECT striatal asymmetry index and cardiac (123)I-metaiodobenzylguanidine scintigraphy examinations for diagnosis of parkinsonisms. J Neurol Sci 377:174–178PubMedCrossRef
86.
Nuvoli S, Palumbo B, Malaspina S, Madeddu G, Spanu A (2018) (123)I-ioflupane SPET and (123)I-MIBG in the diagnosis of Parkinson’s disease and parkinsonian disorders and in the differential diagnosis between Alzheimer’s and Lewy’s bodies dementias. Hell J Nucl Med 21:60–68PubMed
87.
Nuvoli S, Spanu A, Piras MR, Nieddu A, Mulas A, Rocchitta G, Galleri G, Serra PA, Madeddu G (2017) 123I-ioflupane brain SPECT and 123I-MIBG cardiac planar scintigraphy combined use in uncertain parkinsonian disorders. Medicine (Baltimore) 96:e6967CrossRef
88.
Odagiri H, Baba T, Nishio Y, Iizuka O, Matsuda M, Inoue K, Kikuchi A, Hasegawa T, Aoki M, Takeda A, Taki Y, Mori E (2016) On the utility of MIBG SPECT/CT in evaluating cardiac sympathetic dysfunction in Lewy body diseases. PLoS One 11:e0152746PubMedPubMedCentralCrossRef
89.
Oka H, Mochio S, Yoshioka M, Morita M, Onouchi K, Inoue K (2006) Cardiovascular dysautonomia in Parkinson’s disease and multiple system atrophy. Acta Neurol Scand 113:221–227PubMedCrossRef
90.
Okishige K, Sasano T, Yano K, Azegami K, Suzuki K, Itoh K (2001) Serious arrhythmias in patients with apical hypertrophic cardiomyopathy. Intern Med 40:396–402PubMedCrossRef
91.
Orimo S, Amino T, Itoh Y, Takahashi A, Kojo T, Uchihara T, Tsuchiya K, Mori F, Wakabayashi K, Takahashi H (2005) Cardiac sympathetic denervation precedes neuronal loss in the sympathetic ganglia in Lewy body disease. Acta Neuropathol 109:583–588PubMedCrossRef
92.
Orimo S, Kanazawa T, Nakamura A, Uchihara T, Mori F, Kakita A, Wakabayashi K, Takahashi H (2007) Degeneration of cardiac sympathetic nerve can occur in multiple system atrophy. Acta Neuropathol 113:81–86PubMedCrossRef
93.
Orimo S, Oka T, Miura H, Tsuchiya K, Mori F, Wakabayashi K, Nagao T, Yokochi M (2002) Sympathetic cardiac denervation in Parkinson’s disease and pure autonomic failure but not in multiple system atrophy. J Neurol Neurosurg Psychiatry 73:776–777PubMedPubMedCentralCrossRef
94.
Orimo S, Suzuki M, Inaba A, Mizusawa H (2012) 123I-MIBG myocardial scintigraphy for differentiating Parkinson’s disease from other neurodegenerative parkinsonism: a systematic review and meta-analysis. Parkinsonism Relat Disord 18:494–500PubMedCrossRef
95.
Pandit-Taskar N, Zanzonico P, Staton KD, Carrasquillo JA, Reidy-Lagunes D, Lyashchenko S, Burnazi E, Zhang H, Lewis JS, Blasberg R, Larson SM, Weber WA, Modak S (2018) Biodistribution and dosimetry of (18)F-meta-fluorobenzylguanidine: a first-in-human PET/CT imaging study of patients with neuroendocrine malignancies. J Nucl Med 59:147–153PubMedPubMedCentralCrossRef
96.
Raffel DM, Koeppe RA, Little R, Wang CN, Liu S, Junck L, Heumann M, Gilman S (2006) PET measurement of cardiac and nigrostriatal denervation in parkinsonian syndromes. J Nucl Med 47:1769–1777PubMed
97.
Rascol O, Schelosky L (2009) 123I-metaiodobenzylguanidine scintigraphy in Parkinson’s disease and related disorders. Mov Disord 24[Suppl 2]:S732–S741PubMedCrossRef
98.
Reinhardt MJ, Jungling FD, Krause TM, Braune S (2000) Scintigraphic differentiation between two forms of primary dysautonomia early after onset of autonomic dysfunction: value of cardiac and pulmonary iodine-123 MIBG uptake. Eur J Nucl Med 27:595–600PubMedCrossRef
99.
Rundqvist B, Bergmann-Sverrisdottir Y, Andersson B, Elam M, Eisenhofer G, Waagstein F, Friberg P (2001) Metoprolol reduces sympathetic nerve hyperactivity in patients with heart failure. J Heart Lung Transplant 20:251–252PubMedCrossRef
100.
Rundqvist B, Elam M, Bergmann-Sverrisdottir Y, Eisenhofer G, Friberg P (1997) Increased cardiac adrenergic drive precedes generalized sympathetic activation in human heart failure. Circulation 95:169–175PubMedCrossRef
101.
Saiki S, Hirose G, Sakai K, Kataoka S, Hori A, Saiki M, Kaito M, Higashi K, Taki S, Kakeshita K, Fujino S, Miaki M (2004) Cardiac 123I-MIBG scintigraphy can assess the disease severity and phenotype of PD. J Neurol Sci 220:105–111PubMedCrossRef
102.
Sestini S, Pestelli F, Leoncini M, Bellandi F, Mazzeo C, Mansi L, Carrio I, Castagnoli A (2017) The natural history of takotsubo syndrome: a 2-year follow-up study with myocardial sympathetic and perfusion G-SPECT imaging. Eur J Nucl Med Mol Imaging 44:267–283PubMedCrossRef
103.
Sharabi Y, Eldadah B, Li ST, Dendi R, Pechnik S, Holmes C, Goldstein DS (2006) Neuropharmacologic distinction of neurogenic orthostatic hypotension syndromes. Clin Neuropharmacol 29:97–105PubMedCrossRef
104.
Shinohara H, Fukuda N, Soeki T, Sakabe K, Onose Y, Tamura Y (2002) Effects of angiotensin II receptor antagonists on [(123)I]metaiodobenzylguanidine myocardial imaging findings and neurohumoral factors in chronic heart failure. Heart Vessels 17:47–52PubMedCrossRef
105.
Shulkin BL, Shapiro B, Tobes MC, Shen SW, Wieland DM, Meyers LJ, Lee HT, Petry NA, Sisson JC, Beierwaltes WH (1986) Iodine-123-4-amino-3-iodobenzylguanidine, a new sympathoadrenal imaging agent: comparison with iodine-123 metaiodobenzylguanidine. J Nucl Med 27:1138–1142PubMed
106.
Sisson JC, Frager MS, Valk TW, Gross MD, Swanson DP, Wieland DM, Tobes MC, Beierwaltes WH, Thompson NW (1981) Scintigraphic localization of pheochromocytoma. N Engl J Med 305:12–17PubMedCrossRef
107.
Sisson JC, Shapiro B, Meyers L, Mallette S, Mangner TJ, Wieland DM, Glowniak JV, Sherman P, Beierwaltes WH (1987) Metaiodobenzylguanidine to map scintigraphically the adrenergic nervous system in man. J Nucl Med 28:1625–1636PubMed
108.
109.
Soeki T, Tamura Y, Bandou K, Tanaka H, Takeichi N, Shinohara H, Yui Y, Fukuda N, Sui O (1998) Long-term effects of the angiotensin-converting enzyme inhibitor enalapril on chronic heart failure. Examination by 123I-MIBG imaging. Jpn Heart J 39:743–751PubMedCrossRef
110.
Somsen GA, van Vlies B, de Milliano PA, Borm JJ, van Royen EA, Endert E, Lie KI (1996) Increased myocardial [123I]-metaiodobenzylguanidine uptake after enalapril treatment in patients with chronic heart failure. Heart 76:218–222PubMedPubMedCentralCrossRef
111.
Sonni I, Ratib O, Boccardi M, Picco A, Herholz K, Nobili F, Varrone A, Force Geneva Task, for the Roadmap of Alzheimer’s B (2017) Clinical validity of presynaptic dopaminergic imaging with (123)I-ioflupane and noradrenergic imaging with (123)I-MIBG in the differential diagnosis between Alzheimer’s disease and dementia with Lewy bodies in the context of a structured 5-phase development framework. Neurobiol Aging 52:228–242PubMedCrossRef
112.
Stevens MJ, Dayanikli F, Raffel DM, Allman KC, Sandford T, Feldman EL, Wieland DM, Corbett J, Schwaiger M (1998) Scintigraphic assessment of regionalized defects in myocardial sympathetic innervation and blood flow regulation in diabetic patients with autonomic neuropathy. J Am Coll Cardiol 31:1575–1584PubMedCrossRef
113.
Suzuki M, Kurita A, Hashimoto M, Fukumitsu N, Abo M, Ito Y, Urashima M, Inoue K (2006) Impaired myocardial 123I-metaiodobenzylguanidine uptake in Lewy body disease: comparison between dementia with Lewy bodies and Parkinson’s disease. J Neurol Sci 240:15–19PubMedCrossRef
114.
Takahashi M, Ikemura M, Oka T, Uchihara T, Wakabayashi K, Kakita A, Takahashi H, Yoshida M, Toru S, Kobayashi T, Orimo S (2015) Quantitative correlation between cardiac MIBG uptake and remaining axons in the cardiac sympathetic nerve in Lewy body disease. J Neurol Neurosurg Psychiatry 86:939–944PubMedCrossRef
115.
Taki J, Yoshita M, Yamada M, Tonami N (2004) Significance of 123I-MIBG scintigraphy as a pathophysiological indicator in the assessment of Parkinson’s disease and related disorders: it can be a specific marker for Lewy body disease. Ann Nucl Med 18:453–461PubMedCrossRef
116.
Tipre DN, Goldstein DS (2005) Cardiac and extra-cardiac sympathetic denervation in Parkinson disease with orthostatic hypotension and in pure autonomic failure. J Nucl Med 46:1775–1781PubMed
117.
Toru S, Kanouchi T, Yokota T, Yagi Y, Machida A, Kobayashi T (2018) Utility of autonomic function tests to differentiate dementia with Lewy bodies and Parkinson disease with dementia from Alzheimer disease. Eur Neurol 79:27–32PubMedCrossRef
118.
Toyama T, Hoshizaki H, Seki R, Isobe N, Adachi H, Naito S, Oshima S, Taniguchi K (2003) Efficacy of carvedilol treatment on cardiac function and cardiac sympathetic nerve activity in patients with dilated cardiomyopathy: comparison with metoprolol therapy. J Nucl Med 44:1604–1611PubMed
119.
Treglia G, Cason E, Gabellini A, Giordano A, Fagioli G (2010) Recent developments in innervation imaging using iodine-123-metaiodobenzylguanidine scintigraphy in Lewy body diseases. Neurol Sci 31:417–422PubMedCrossRef
120.
Treglia G, Cason E, Giordano A, Fagioli G (2012) Abnormal striatal dopaminergic and cardiac sympathetic imaging in dementia with Lewy bodies: two sides of the same coin. Parkinsonism Relat Disord 18:707–708 (author reply 709)PubMedCrossRef
121.
Treglia G, Stefanelli A, Cason E, Cocciolillo F, Di Giuda D, Giordano A (2011) Diagnostic performance of iodine-123-metaiodobenzylguanidine scintigraphy in differential diagnosis between Parkinson’s disease and multiple-system atrophy: a systematic review and a meta-analysis. Clin Neurol Neurosurg 113:823–829PubMedCrossRef
122.
Umemura A, Oeda T, Hayashi R, Tomita S, Kohsaka M, Yamamoto K, Sawada H (2013) Diagnostic accuracy of apparent diffusion coefficient and 123I-metaiodobenzylguanidine for differentiation of multiple system atrophy and Parkinson’s disease. PLoS One 8:e61066PubMedPubMedCentralCrossRef
123.
Uyama N, Otsuka H, Shinya T, Otomi Y, Harada M, Sako W, Izumi Y, Kaji R, Watanabe Y, Takashi S, Kunikane Y (2017) The utility of the combination of a SPECT study with [123I]-FP-CIT of dopamine transporters and [123I]-MIBG myocardial scintigraphy in differentiating Parkinson disease from other degenerative parkinsonian syndromes. Nucl Med Commun 38:487–492PubMedPubMedCentralCrossRef
124.
Valli N, Labrousse L, Reant P, Dos-Santos P (2007) Significant improvement of cardiac sympathetic function following cardiac support device implantation: illustration by 123I-MIBG scintigraphy. Eur J Cardiothorac Surg 32:943–944PubMedCrossRef
125.
126.
Villarroel AH, Vitola JV, Stier AL Jr, Dippe T Jr, Cunha C (2009) Takotsubo or stress cardiomyopathy: role of nuclear cardiology using (123)I-MIBG. Expert Rev Cardiovasc Ther 7:847–852PubMedCrossRef
127.
Vinik AI, Maser RE, Mitchell BD, Freeman R (2003) Diabetic autonomic neuropathy. Diabetes Care 26:1553–1579PubMedCrossRef
128.
Wakabayashi T, Nakata T, Hashimoto A, Yuda S, Tsuchihashi K, Travin MI, Shimamoto K (2001) Assessment of underlying etiology and cardiac sympathetic innervation to identify patients at high risk of cardiac death. J Nucl Med 42:1757–1767PubMed
129.
Wieland DM, Brown LE, Rogers WL, Worthington KC, Wu JL, Clinthorne NH, Otto CA, Swanson DP, Beierwaltes WH (1981) Myocardial imaging with a radioiodinated norepinephrine storage analog. J Nucl Med 22:22–31PubMed
130.
Wittstein IS, Thiemann DR, Lima JA, Baughman KL, Schulman SP, Gerstenblith G, Wu KC, Rade JJ, Bivalacqua TJ, Champion HC (2005) Neurohumoral features of myocardial stunning due to sudden emotional stress. N Engl J Med 352:539–548PubMedCrossRef
131.
Wong KK, Raffel DM, Koeppe RA, Frey KA, Bohnen NI, Gilman S (2012) Pattern of cardiac sympathetic denervation in idiopathic Parkinson disease studied with 11C hydroxyephedrine PET. Radiology 265:240–247PubMedPubMedCentralCrossRef
132.
133.
Shams Y-H, Tornvall P (2018) Epidemiology, pathogenesis, and management of takotsubo syndrome. Clin Auton Res 28:53–65CrossRef
134.
Yang T, Wang L, Li Y, Cheng M, Jiao J, Wang Q, Guo H (2017) (131)I-MIBG myocardial scintigraphy for differentiation of Parkinson’s disease from multiple system atrophy or essential tremor in Chinese population. J Neurol Sci 373:48–51PubMedCrossRef
135.
Yoshita M, Arai H, Arai H, Arai T, Asada T, Fujishiro H, Hanyu H, Iizuka O, Iseki E, Kashihara K, Kosaka K, Maruno H, Mizukami K, Mizuno Y, Mori E, Nakajima K, Nakamura H, Nakano S, Nakashima K, Nishio Y, Orimo S, Samuraki M, Takahashi A, Taki J, Tokuda T, Urakami K, Utsumi K, Wada K, Washimi Y, Yamasaki J, Yamashina S, Yamada M (2015) Diagnostic accuracy of 123I-meta-iodobenzylguanidine myocardial scintigraphy in dementia with Lewy bodies: a multicenter study. PLoS One 10:e0120540PubMedPubMedCentralCrossRef
136.
Yoshita M, Taki J, Yamada M (2001) A clinical role for [(123)I]MIBG myocardial scintigraphy in the distinction between dementia of the Alzheimer’s-type and dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 71:583–588PubMedPubMedCentralCrossRef
137.
Yoshita M, Taki J, Yokoyama K, Noguchi-Shinohara M, Matsumoto Y, Nakajima K, Yamada M (2006) Value of 123I-MIBG radioactivity in the differential diagnosis of DLB from AD. Neurology 66:1850–1854PubMedCrossRef
Metadata
Title
Roles of cardiac sympathetic neuroimaging in autonomic medicine
Authors
David S. Goldstein
William P. Cheshire Jr.
Publication date
01-08-2018
Publisher
Springer Berlin Heidelberg
Published in
Clinical Autonomic Research / Issue 4/2018
Print ISSN: 0959-9851
Electronic ISSN: 1619-1560
DOI
https://doi.org/10.1007/s10286-018-0547-6

Other articles of this Issue 4/2018

Clinical Autonomic Research 4/2018 Go to the issue

Editorial

Maintaining cerebral oxygen homeostasis: a serious business

Consensus Statement

Consensus statement on the definition of neurogenic supine hypertension in cardiovascular autonomic failure by the American Autonomic Society (AAS) and the European Federation of Autonomic Societies (EFAS)

Review

Gastrointestinal symptoms in postural tachycardia syndrome: a systematic review

Research Article

Ambulatory blood pressure profiles in familial dysautonomia

Correction

Correction to: Risk reduction of long-term major adverse cardiovascular events after endoscopic thoracic sympathectomy in palmar hyperhidrosis

Review

Neurogenic hypertension: pathophysiology, diagnosis and management