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Semin Neurol 2003; 23(4): 423-434
DOI: 10.1055/s-2004-817726
DOI: 10.1055/s-2004-817726
Imaging of the Autonomic Nervous System: Focus on Cardiac Sympathetic Innervation
David S. Goldstein- Clinical Neurocardiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
Further Information
Publication History
Publication Date:
15 April 2004 (online)
ABSTRACT
Symptoms or signs of abnormal autonomic nervous system function occur commonly in several neurological disorders. Clinical evaluations have depended on physiological, pharmacological, and neurochemical approaches. Recently, imaging of sympathetic noradrenergic innervation has been introduced and applied especially in the heart. Most studies have used the radiolabeled sympathomimetic amine, 123I-metaiodobenzylguanidine. Decreased uptake or increased “washout” of 123I-metaiodobenzylguanidine-derived radioactivity is associated with worse prognosis or more severe disease in hypertension, congestive heart failure, arrhythmias, and diabetes mellitus. This pattern may reflect a high rate of postganglionic sympathetic nerve traffic to the heart. Many recent studies have agreed on the remarkable finding that all patients with Parkinson's disease and orthostatic hypotension have a loss of cardiac sympathetic innervation, whereas all patients with multiple system atrophy, often difficult to distinguish clinically from Parkinson's disease, have intact cardiac sympathetic innervation. Because Parkinson's disease entails a postganglionic sympathetic noradrenergic lesion, the disease appears to be not only a movement disorder, with dopamine loss in the nigrostriatal system of the brain, but also a dysautonomia, with noradrenaline loss in the sympathetic nervous system of the heart. As new ligands are developed, one may predict further discoveries of involvement of components of the autonomic nervous system in neurological diseases.
KEYWORDS
Sympathetic - multiple system atrophy - Parkinson's disease - autonomic failure - norepinephrine - dysautonomia
REFERENCES
- 1 Goldstein D, Eisenhofer G, Robertson D, Straus R, Esler M. Dysautonomias: clinical disorders of the autonomic nervous system. Ann Intern Med . 2002; 137 753-763
- 2 Goldstein D S. The Autonomic Nervous System in Health and Disease. New York: Marcel Dekker, Inc 2001
- 3 Pacak K, Palkovits M, Yadid G, Kvetnansky R, Kopin I J, Goldstein D S. Heterogeneous neurochemical responses to different stressors: a test of Selye's doctrine of nonspecificity. Am J Physiol . 1998; 275 R1247-R1255
- 4 Young J B, Rosa R M, Landsberg L. Dissociation of sympathetic nervous system and adrenal medullary responses. Am J Physiol . 1984; 247 E35-E40
- 5 Oliver G, Schafer E A. On the physiological action of extract of the suprarenal capsules. J Physiol . 1895; 17 ix-xiv
- 6 Abel J J, Crawford A C. On the blood-pressure-raising constituent of the suprarenal capsule. Bull Johns Hopkins Hosp . 1897; 8 151-157
- 7 Abel J J. On a simple method of preparing epinephrin and its compounds. Bull Johns Hopkins Hosp . 1902; 13 29-36
- 8 Takamine J. The isolation of the active principle of the suprarenal gland. J Physiol . 1901; 27 30P-39P
- 9 Goldstein D S, Tack C. Non-invasive detection of sympathetic neurocirculatory failure. Clin Auton Res . 2000; 10 285-291
- 10 Bootsma M, Swenne C A, Van Bolhuis H H, Chang P C, Cats V M, Bruschke A V. Heart rate and heart rate variability as indexes of sympathovagal balance. Am J Physiol . 1994; 266 H1565-H1571
- 11 Grassi G, Esler M. How to assess sympathetic activity in humans. J Hypertens . 1999; 17 719-734
- 12 Hagbarth K E, Burke D. Microneurography in man. Acta Neurol (Napoli) . 1977; 32 30-34
- 13 Wallin B G, Elam M. Microneurography and autonomic dysfunction. In: Low PA, ed. Clinical Autonomic Disorders Boston: Little, Brown 1993: 243-252
- 14 Dale H H. The action of certain esters and ethers of choline, and their relation to muscarine. J Pharmacol Exp Ther . 1914; 6 147-190
- 15 Loewi O, Navratil E. Uber humorale Ubertragbarkeit der Herzenvenwirkung. X. Mitteilung. Uber das Schicksal des Vagusstoffs. Pflugers Arch . 1926; 214 678-688
- 16 Ahlquist R P. A study of adrenotropic receptors. Am J Physiol . 1948; 153 586-600
- 17 Polinsky R J, Kopin I J, Ebert M H, Weise V. Pharmacologic distinction of different orthostatic hypotension syndromes. Neurology . 1981; 31 1-7
- 18 Bianchetti M G, Minder I, Beretta-Piccoli C, Meier A, Weidmann P. Effects of tyramine on blood pressure and plasma catecholamines in normal and hypertensive subjects. Klin Wochenschr . 1982; 60 465-470
- 19 Shannon J R, Flattem N L, Jordan J. et al . Orthostatic intolerance and tachycardia associated with norepinephrine-transporter deficiency. N Engl J Med . 2000; 342 541-549
- 20 Jordan J, Shannon J R, Black B K. et al . N(N)-nicotinic blockade as an acute human model of autonomic failure. Hypertension . 1998; 31 1178-1184
- 21 Goldstein D S, Grossman E, Listwak S, Folio C J. Sympathetic reactivity during a yohimbine challenge test in essential hypertension. Hypertension . 1991; 18(Suppl. III) 40-48
- 22 Charney D S, Heninger G R, Redmond Jr E D. Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci . 1983; 33 19-29
- 23 Senard J M, Rascol O, Durrieu G. et al . Effects of yohimbine on plasma catecholamine levels in orthostatic hypotension related to Parkinson disease or multiple system atrophy. Clin Neuropharmacol . 1993; 16 70-76
- 24 Biaggioni I, Robertson R M, Robertson D. Manipulation of norepinephrine metabolism with yohimbine in the treatment of autonomic failure. J Clin Pharmacol . 1994; 34 418-423
- 25 Goldstein D S, Keiser H R. Pressor and depressor responses after cholinergic blockade in humans. Am Heart J . 1984; 107(5 Pt 1) 974-979
- 26 Bristow J D, Honour J, Pickering G W, Sleight P, Smyth H S. Diminished baroreflex sensitivity in high blood pressure. Circulation . 1969; 39 48-54
- 27 Cannon W B, de la Paz D. Emotional stimulation of adrenal gland secretion. Am J Physiol . 1911; 28 64-70
- 28 Cannon W B. The emergency function of the adrenal medulla in pain and in the major emotions. Am J Physiol . 1914; 33 356-372
- 29 Cannon W B. The interrelation of emotions as suggested by recent physiological researches. Am J Psychol . 1914; 25 256-282
- 30 Cannon W B, Rapport D. Further observations on the denervated heart in relation to adrenal secretion. Am J Physiol . 1921; 58 308-337
- 31 Goldstein D S, Feuerstein G, Izzo Jr L J, Kopin I J, Keiser H R. Validity and reliability of liquid chromatography with electrochemical detection for measuring plasma levels of norepinephrine and epinephrine in man. Life Sci . 1981; 28 467-475
- 32 Holmes C, Eisenhofer G, Goldstein D S. Improved assay for plasma dihydroxyphenylacetic acid and other catechols using high-performance liquid chromatography with electrochemical detection. J Chromatogr B Biomed Appl . 1994; 653 131-138
- 33 Eisenhofer G, Goldstein D S, Stull R. et al . Simultaneous liquid-chromatographic determination of 3,4-dihydroxyphenylglycol, catecholamines, and 3,4-dihydroxyphenylalanine in plasma, and their responses to inhibition of monoamine oxidase. Clin Chem . 1986; 32 2030-2033
- 34 Kuwahara T, Hamada M, Hiwada K. Direct evidence of impaired cardiac sympathetic innervation in essential hypertensive patients with left ventricular hypertrophy. J Nucl Med . 1998; 39 1486-1491
- 35 Sakata K, Shirotani M, Yoshida H, Kurata C. Cardiac sympathetic nervous system in early essential hypertension assessed by 123I-MIBG. J Nucl Med . 1999; 40 6-11
- 36 Watanabe K, Sekiya M, Tsuruoka T. et al . Relationship between insulin resistance and cardiac sympathetic nervous function in essential hypertension. J Hypertens . 1999; 17 1161-1168
- 37 Ohya Y, Sasaki M, Fujishima S. et al . Myocardial imaging with 123I-metaiodobenzylguanidine in essential hypertension and renovascular hypertension. Clin Exp Hypertens . 2001; 23 293-304
- 38 Takahashi N, Nakagawa M, Saikawa T. et al . Effect of essential hypertension on cardiac autonomic function in type 2 diabetic patients. J Am Coll Cardiol . 2001; 38 232-237
- 39 Simula S, Vanninen E, Viitanen L. et al . Cardiac adrenergic innervation is affected in asymptomatic subjects with very early stage of coronary artery disease. J Nucl Med . 2002; 43 1-7
- 40 Agostini D, Lecluse E, Belin A. et al . Impact of exercise rehabilitation on cardiac neuronal function in heart failure: an iodine-123 metaiodobenzylguanidine scintigraphy study. Eur J Nucl Med . 1998; 25 235-241
- 41 Kurata C, Shouda S, Mikami T. et al . Metaiodobenzylguanidine and heart rate variability in heart failure. Jpn Circ J . 1998; 62 770-772
- 42 Atsumi H, Takeishi Y, Fujiwara S, Tomoike H. Cardiac sympathetic nervous disintegrity is related to exercise intolerance in patients with chronic heart failure. Nucl Med Commun . 1998; 19 451-456
- 43 Merlet P, Pouillart F, Dubois-Rande J L. et al . Sympathetic nerve alterations assessed with 123I-MIBG in the failing human heart. J Nucl Med . 1999; 40 224-231
- 44 Sakamaki F, Satoh T, Nagaya N. et al . Correlation between severity of pulmonary arterial hypertension and 123I-metaiodobenzylguanidine left ventricular imaging. J Nucl Med . 2000; 41 1127-1133
- 45 de Milliano A P, van Eck-Smit L B, van Zwieten A P, de Groot C A, Tijssen J G, Lie K I. Relationship between cardiac metaiodobenzylguanidine uptake and hemodynamic, functional and neurohormonal parameters in patients with heart failure. Eur J Heart Fail . 2001; 3 693-697
- 46 de Milliano A P, Tijssen J G, van Eck-Smit L B, Lie K I. Cardiac 123 I-MIBG imaging and clinical variables in risk stratification in patients with heart failure treated with beta blockers. Nucl Med Commun . 2002; 23 513-519
- 47 Takahashi N, Ishida Y, Maeno M. et al . Noninvasive identification of left ventricular involvements in arrhythmogenic right ventricular dysplasia: comparison of 123I-MIBG, 201TlCl, magnetic resonance imaging and ultrafast computed tomography. Ann Nucl Med . 1997; 11 233-241
- 48 Yukinaka M, Nomura M, Ito S, Nakaya Y. Mismatch between myocardial accumulation of 123I-MIBG and 99mTc-MIBI and late ventricular potentials in patients after myocardial infarction: association with the development of ventricular arrhythmias. Am Heart J . 1998; 136 859-867
- 49 Nomura M, Nada T, Endo J. et al . Brugada syndrome associated with an autonomic disorder. Heart . 1998; 80 194-196
- 50 Schafers M, Wichter T, Lerch H. et al . Cardiac 123I-MIBG uptake in idiopathic ventricular tachycardia and fibrillation. J Nucl Med . 1999; 40 1-5
- 51 Okishige K, Sasano T, Yano K, Azegami K, Suzuki K, Itoh K. Serious arrhythmias in patients with apical hypertrophic cardiomyopathy. Intern Med . 2001; 40 396-402
- 52 Wichter T, Matheja P, Eckardt L. et al . Cardiac autonomic dysfunction in Brugada syndrome. Circulation . 2002; 105 702-706
- 53 Nagaoka H, Iizuka T, Kubota S. et al . Depressed contractile response to exercise in diabetic patients in the absence of cardiovascular disease: relationship to adrenergic cardiac dysinnervation. Nucl Med Commun . 1997; 18 761-770
- 54 Ziegler D, Weise F, Langen K J. et al . Effect of glycaemic control on myocardial sympathetic innervation assessed by [123I]metaiodobenzylguanidine scintigraphy: a 4-year prospective study in IDDM patients. Diabetologia . 1998; 41 443-451
- 55 Nagamachi S, Jinnouchi S, Kurose T. et al . 123I-MIBG myocardial scintigraphy in diabetic patients: relationship with 201Tl uptake and cardiac autonomic function. Ann Nucl Med . 1998; 12 323-331
- 56 Uehara A, Kurata C, Sugi T, Mikami T, Shouda S. Diabetic cardiac autonomic dysfunction: parasympathetic versus sympathetic. Ann Nucl Med . 1999; 13 95-100
- 57 Giordano A, Calcagni M L, Verrillo A. et al . Assessment of sympathetic innervation of the heart in diabetes mellitus using 123I-MIBG. Diabetes Nutr Metab . 2000; 13 350-355
- 58 Nagamachi S, Jinnouchi S, Kurose T. et al . Serial change in 123I-MIBG myocardial scintigraphy in non-insulin-dependent diabetes mellitus. Ann Nucl Med . 2002; 16 33-38
- 59 Hattori N, Rihl J, Bengel F M. et al . Cardiac autonomic dysinnervation and myocardial blood flow in long-term type 1 diabetic patients. Diabet Med . 2003; 20 375-381
- 60 Agostini D, Babatasi G, Manrique A. et al . Impairment of cardiac neuronal function in acute myocarditis: iodine-123-MIBG scintigraphy study. J Nucl Med . 1998; 39 1841-1844
- 61 Kakuchi H, Sasaki T, Ishida Y, Komamura K, Miyatake K. 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 . 1999; 81 148-152
- 62 Toyama T, Aihara Y, Iwasaki T. et al . Cardiac sympathetic activity estimated by 123I-MIBG myocardial imaging in patients with dilated cardiomyopathy after beta-blocker or angiotensin-converting enzyme inhibitor therapy. J Nucl Med . 1999; 40 217-223
- 63 Momose M, Kobayashi H, Iguchi N. et al . Comparison of parameters of 123I-MIBG scintigraphy for predicting prognosis in patients with dilated cardiomyopathy. Nucl Med Commun . 1999; 20 529-535
- 64 Merlet P, Benvenuti C, Moyse D. et al . Prognostic value of MIBG imaging in idiopathic dilated cardiomyopathy. J Nucl Med . 1999; 40 917-923
- 65 Maunoury C, Agostini D, Acar P. et al . Impairment of cardiac neuronal function in childhood dilated cardiomyopathy: an 123I-MIBG scintigraphic study. J Nucl Med . 2000; 41 400-404
- 66 Naruse H, Arii T, Kondo T. et al . Relation between myocardial response to dobutamine stress and sympathetic nerve activation in patients with idiopathic dilated cardiomyopathy: a comparison of 123I-MIBG scintigraphic and echocardiographic data. Ann Nucl Med . 2000; 14 427-432
- 67 Matsui T, Tsutamoto T, Kinoshita M. Relationship between cardiac 123I-metaiodobenzylguanidine imaging and the transcardiac gradient of neurohumoral factors in patients with dilated cardiomyopathy. Jpn Circ J . 2001; 65 1041-1046
- 68 Shimizu M, Ino H, Yamaguchi M. et al . Heterogeneity of cardiac sympathetic nerve activity and systolic dysfunction in patients with hypertrophic cardiomyopathy. J Nucl Med . 2002; 43 15-20
- 69 Matsui T, Tsutamoto T, Maeda K, Kusukawa J, Kinoshita M. 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 . 2002; 66 537-543
- 70 Kasama S, Toyama T, Hoshizaki H. et al . Dobutamine gated blood pool scintigraphy predicts the improvement of cardiac sympathetic nerve activity, cardiac function, and symptoms after treatment in patients with dilated cardiomyopathy. Chest . 2002; 122 542-548
- 71 Lanza G A. Abnormal cardiac nerve function in syndrome X. Herz . 1999; 24 97-106
- 72 Lanza G A, Giordano A, Pristipino C. et al . Relationship between myocardial 123I-metaiodobenzylguanidine scintigraphic uptake and heart rate variability in patients with syndrome X. Ital Heart J . 2000; 1 221-225
- 73 Abe Y, Sugiura T, Takehana K. et al . Clinical significance of denervated but viable myocardium in patients with recanalized acute myocardial infarction. Nucl Med Commun . 1999; 20 727-735
- 74 Bengel F M, Barthel P, Matsunari I, Schmidt G, Schwaiger M. Kinetics of 123I-MIBG after acute myocardial infarction and reperfusion therapy. J Nucl Med . 1999; 40 904-910
- 75 Ando M, Yamabe H, Sakurai K, Kawai H, Yokoyama M. Relationship between cardiac sympathetic function and baroreceptor sensitivity after acute myocardial infarction. Circ J . 2002; 66 247-252
- 76 Soeki T, Tamura Y, Bandou K. et al . Long-term effects of the angiotensin-converting enzyme inhibitor enalapril on chronic heart failure. Examination by 123I-MIBG imaging. Jpn Heart J . 1998; 39 743-751
- 77 Sakata K, Shirotani M, Yoshida H. et al . Effects of amlodipine and cilnidipine on cardiac sympathetic nervous system and neurohormonal status in essential hypertension. Hypertension . 1999; 33 1447-1452
- 78 Agostini D, Belin A, Amar M H. et al . Improvement of cardiac neuronal function after carvedilol treatment in dilated cardiomyopathy: a 123I-MIBG scintigraphic study. J Nucl Med . 2000; 41 845-851
- 79 Lotze U, Kaepplinger S, Kober A, Richartz B M, Gottschild D, Figulla H R. Recovery of the cardiac adrenergic nervous system after long-term beta-blocker therapy in idiopathic dilated cardiomyopathy: assessment by increase in myocardial 123I-metaiodobenzylguanidine uptake. J Nucl Med . 2001; 42 49-54
- 80 de Milliano A P, de Groot C A, Tijssen J G, van Eck-Smit L B, Van Zwieten A P, Lie K I. Beneficial effects of metoprolol on myocardial sympathetic function: evidence from a randomized, placebo-controlled study in patients with congestive heart failure. Am Heart J . 2002; 144 E3
- 81 Goldstein D S, Katzper M, Linares O A, Kopin I J. Kinetic model for the fate of the sympathoneural imaging agent 6[18F]fluorodopamine in the human heart: a novel means to assess cardiac sympathetic neuronal function. Naunyn Schmiedebergs Arch Pharmacol . 2002; 365 38-49
- 82 Shouda S, Kurata C, Mikami T, Wakabayashi Y. Effects of extrinsically elevated plasma norepinephrine concentration on myocardial 123I-MIBG kinetics in rats. J Nucl Med . 1999; 40 2088-2093
- 83 Senard J M, Rai S, Lapeyre-Mestre M. et al . Prevalence of orthostatic hypotension in Parkinson's disease. J Neurol Neurosurg Psychiatry . 1997; 63 584-589
- 84 Micieli G, Martignoni E, Cavallini A, Sandrini G, Nappi G. Postprandial and orthostatic hypotension in Parkinson's disease. Neurology . 1987; 37 386-393
- 85 Anonymous. Cardiovascular disorders in Parkinson disease are underrated. Fortschr Neurol Psychiatr . 1999; 67 A8-A9
- 86 Hillen M E, Wagner M L, Sage J I. “Subclinical” orthostatic hypotension is associated with dizziness in elderly patients with Parkinson disease. Arch Phys Med Rehabil . 1996; 77 710-712
- 87 Gilman S, Low P, Quinn N. et al . Consensus statement on the diagnosis of multiple system atrophy. Clin Auton Res . 1998; 8 359-362
- 88 Mathias C J. The classification and nomenclature of autonomic disorders-ending chaos, resolving conflict and hopefully achieving clarity. Clin Auton Res . 1995; 5 307-310
- 89 Goldstein D S, Polinsky R J, Garty M. et al . Patterns of plasma levels of catechols in neurogenic orthostatic hypotension. Ann Neurol . 1989; 26 558-563
- 90 Goldstein D S, Holmes C, Sharabi Y, Brentzel S, Eisenhofer G. Plasma levels of catechols and metanephrines in neurogenic orthostatic hypotension. Neurology . 2003; 60 1327-1332
- 91 Polinsky R J. Neuropharmacological investigation of autonomic failure. In: Bannister R, Mathias CJ, eds. Autonomic Failure New York: Oxford University Press 1992: 334-358
- 92 Jordan J, Shannon J R, Biaggioni I, Norman R, Black B K, Robertson D. Contrasting actions of pressor agents in severe autonomic failure. Am J Med . 1998; 105 116-124
- 93 Hague K, Lento P, Morgello S, Caro S, Kaufmann H. The distribution of Lewy bodies in pure autonomic failure: autopsy findings and review of the literature. Acta Neuropathol (Berl) . 1997; 94 192-196
- 94 Orimo S, Oka T, Miura H. et al . Sympathetic cardiac denervation in Parkinson's disease and pure autonomic failure but not in multiple system atrophy. J Neurol Neurosurg Psychiatry . 2002; 73 776-777
- 95 Black I B, Petito C K. Catecholamine enzymes in the degenerative neurological disease idiopathic orthostatic hypotension. Science . 1976; 192 910-912
- 96 Satoh A, Serita T, Tsujihata M. Total defect of metaiodobenzylguanidine (MIBG) imaging on heart in Parkinson's disease: assessment of cardiac sympathetic denervation. Nippon Rinsho . 1997; 55 202-206
- 97 Satoh A, Serita T, Seto M. et al . Loss of 123I-MIBG uptake by the heart in Parkinson's disease: assessment of cardiac sympathetic denervation and diagnostic value. J Nucl Med . 1999; 40 371-375
- 98 Druschky A, Hilz M J, Platsch G. et al . Differentiation of Parkinson's disease and multiple system atrophy in early disease stages by means of I-123-MIBG-SPECT. J Neurol Sci . 2000; 175 3-12
- 99 Braune S, Reinhardt M, Schnitzer R, Riedel A, Lucking C H. Cardiac uptake of [123I]MIBG separates Parkinson's disease from multiple system atrophy. Neurology . 1999; 53 1020-1025
- 100 Yoshita M, Hayashi M, Hirai S. Decreased myocardial accumulation of 123I-meta-iodobenzyl guanidine in Parkinson's disease. Nucl Med Commun . 1998; 19 137-142
- 101 Kanzaki N, Sato K, Hayabara T. Improved cardiac iodine-123 metaiodobenzylguanidine accumulation after drug therapy in a patient with Parkinson's disease. Clin Nucl Med . 1997; 22 697-699
- 102 Ohmura M. Loss of 123I-MIBG uptake by the heart in Parkinson's disease: assessment of cardiac sympathetic denervation and diagnostic value. J Nucl Med . 2000; 41 1594-1595
- 103 Reinhardt M J, Jungling F D, Krause T M, Braune S. 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 . 2000; 27 595-600
- 104 Braune S, Reinhardt M, Bathmann J, Krause T, Lehmann M, Lucking C H. Impaired cardiac uptake of meta-[123I]iodobenzylguanidine in Parkinson's disease with autonomic failure. Acta Neurol Scand . 1998; 97 307-314
- 105 Orimo S, Ozawa E, Oka T. et al . Different histopathology accounting for a decrease in myocardial MIBG uptake in PD and MSA. Neurology . 2001; 57 1140-1141
- 106 Senard J M, Brefel-Courbon C, Rascol O, Montastruc J L. Orthostatic hypotension in patients with Parkinson's disease: pathophysiology and management. Drugs Aging . 2001; 18 495-505
- 107 Takatsu H, Nishida H, Matsuo H. et al . Cardiac sympathetic denervation from the early stage of Parkinson's disease: clinical and experimental studies with radiolabeled MIBG. J Nucl Med . 2000; 41 71-77
- 108 Orimo S, Ozawa E, Nakade S, Sugimoto T, Mizusawa H. (123)I-metaiodobenzylguanidine myocardial scintigraphy in Parkinson's disease. J Neurol Neurosurg Psychiatry . 1999; 67 189-194
- 109 Yoshita M, Hayashi M, Hirai S. Iodine 123-labeled meta-iodobenzylguanidine myocardial scintigraphy in the cases of idiopathic Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Rinsho Shinkeigaku . 1997; 37 476-482
- 110 Goldstein D S, Holmes C, Li S T, Bruce S, Metman L V, Cannon R O. Cardiac sympathetic denervation in Parkinson disease. Ann Intern Med . 2000; 133 338-347
- 111 Goldstein D S, Holmes C, Dendi R, Bruce S, Li S-T. Orthostatic hypotension from sympathetic denervation in Parkinson's disease. Neurology . 2002; 58 1247-1255
- 112 Li S T, Dendi R, Holmes C, Goldstein D S. Progressive loss of cardiac sympathetic innervation in Parkinson's disease. Ann Neurol . 2002; 52 220-223
- 113 Goldstein D S, Holmes C, Cannon III O R, Eisenhofer G, Kopin I J. Sympathetic cardioneuropathy in dysautonomias. N Engl J Med . 1997; 336 696-702
- 114 Akincioglu C, Unlu M, Tunc T. Cardiac innervation and clinical correlates in idiopathic Parkinson's disease. Nucl Med Commun . 2003; 24 267-271
- 115 Taki J, Nakajima K, Hwang E H. et al . Peripheral sympathetic dysfunction in patients with Parkinson's disease without autonomic failure is heart selective and disease specific. Eur J Nucl Med . 2000; 27 566-573