123I-Ioflupane SPECT and 18F-FDG PET Combined Use in the Characterization of Movement and Cognitive Associated Disorders in Neurodegenerative Diseases

Author(s): Susanna Nuvoli*, Giovanna Tanda, Maria L. Stazza, Barbara Palumbo, Viviana Frantellizzi, Giuseppe De Vincentis, Angela Spanu, Giuseppe Madeddu

Journal Name: Current Alzheimer Research

Volume 18 , Issue 3 , 2021


  Journal Home
Translate in Chinese
Become EABM
Become Reviewer
Call for Editor

Abstract:

Background: Both movement (MD) and cognitive (CD) disorders can occur associated in some neurodegenerative diseases, such as Parkinson’s disease (PD) and Alzheimer’s disease (AD).

Objective: We further investigated the usefulness of 123I-Ioflupane SPECT and 18F-FDG PET combined use in patients with these disorders in the early stage.

Methods: We retrospectively enrolled twenty-five consecutive patients with MD and CD clinical symptoms of recent appearance. All patients had undergone neurologic examination, neuropsychological tests, and magnetic resonance imaging. 123I-Ioflupane SPECT was performed in all cases, followed by 18F-FDG PET two weeks later. In the two procedures, both qualitative (QL) and quantitative (QN) image analyses were determined.

Results: In patients with both 123I-Ioflupane SPECT and 18F-FDG PET pathologic data, associated dopaminergic and cognitive impairments were confirmed in 56% of cases. Pathologic SPECT with normal PET in 16% of cases could diagnose MD and exclude an associated CD, despite clinical symptoms. On the contrary, normal SPECT with pathologic PET in 28% of cases could exclude basal ganglia damage while confirming CD. QN 123I-Ioflupane SPECT analysis showed better performance than QL since QN correctly characterized two cases of MD with normal QL. Moreover, correct classification of normal metabolism was made only by QN analysis of 18F-FDG PET in four cases, despite suspect areas of hypometabolism at QL.

Conclusion: The combined use of these imaging procedures proved a reliable diagnostic tool to accurately identify and characterize MD and CD in early stage. QN analysis was effective in supporting QL evaluation, and its routine use is suggested, especially with inconclusive QL.

Keywords: Movement disorders, cognitive disorders, 123I-Ioflupane SPECT, 18F-FDG PET, qualitative analysis, quantitative analysis.

[1]
Baldacci F, Lista S, O’Bryant SE, Ceravolo R, Toschi N, Hampel H. Blood-based biomarker screening with agnostic biological definitions for an accurate diagnosis within the dimensional spectrum of neurodegenerative diseases. Methods Mol Biol 2018; 1750: 139-55.
[http://dx.doi.org/10.1007/978-1-4939-7704-8_9] [PMID: 29512070]
[2]
Litvan I, Aarsland D, Adler CH, et al. MDS Task Force on mild cognitive impairment in Parkinson’s disease: Critical review of PD-MCI. Mov Disord 2011; 26(10): 1814-24.
[http://dx.doi.org/10.1002/mds.23823] [PMID: 21661055]
[3]
Foguem C, Manckoundia P. Lewy body disease: Clinical and pathological “Overlap Syndrome” Between Synucleinopathies (Parkinson Disease) and Tauopathies (Alzheimer Disease). Curr Neurol Neurosci Rep 2018; 18(5): 24.
[http://dx.doi.org/10.1007/s11910-018-0835-5] [PMID: 29629495]
[4]
Fares A, Borrmann D. Neurochemical aspects of Alzheimer’s disease and movement disturbances: A theory of β-Amyloid and τ-Protein. Am J Alzheimers Dis Other Demen 2018; 33(8): 535-40.
[http://dx.doi.org/10.1177/1533317518790631] [PMID: 30045626]
[5]
Woodward M, Mackenzie IRA, Hsiung G-YR, Jacova C, Feldman H. Multiple brain pathologies in dementia are common. Eur Geriatr Med 2010; 5(1): 259-65.
[http://dx.doi.org/10.1016/j.eurger.2010.07.012]
[6]
Das S, Zhang Z, Ang LC. Clinicopathological overlap of neurodegenerative diseases: A comprehensive review. J Clin Neurosci 2020; 78: 30-3.
[7]
Adler CH, Beach TG, Hentz JG, et al. Low clinical diagnostic accuracy of early vs advanced Parkinson disease: clinicopathologic study. Neurology 2014; 83(5): 406-12.
[http://dx.doi.org/10.1212/WNL.0000000000000641] [PMID: 24975862]
[8]
Joutsa J, Gardberg M, Röyttä M, Kaasinen V. Diagnostic accuracy of parkinsonism syndromes by general neurologists. Parkinsonism Relat Disord 2014; 20(8): 840-4.
[http://dx.doi.org/10.1016/j.parkreldis.2014.04.019] [PMID: 24816002]
[9]
Tolosa E, Wenning G, Poewe W. The diagnosis of Parkinson’s disease. Lancet Neurol 2006; 5(1): 75-86.
[http://dx.doi.org/10.1016/S1474-4422(05)70285-4] [PMID: 16361025]
[10]
Williams DR, Lees AJ. What features improve the accuracy of the clinical diagnosis of progressive supranuclear palsy-parkinsonism (PSP-P)? Mov Disord 2010; 25(3): 357-62.
[http://dx.doi.org/10.1002/mds.22977] [PMID: 20108379]
[11]
Respondek G, Roeber S, Kretzschmar H, et al. Accuracy of the National Institute for Neurological Disorders and Stroke/Society for Progressive Supranuclear Palsy and neuroprotection and natural history in Parkinson plus syndromes criteria for the diagnosis of progressive supranuclear palsy. Mov Disord 2013; 28(4): 504-9.
[http://dx.doi.org/10.1002/mds.25327] [PMID: 23436751]
[12]
Hellwig S, Frings L, Amtage F, et al. 18F-FDG PET is an early predictor of overall survival in suspected atypical parkinsonism. J Nucl Med 2015; 56(10): 1541-6.
[http://dx.doi.org/10.2967/jnumed.115.159822] [PMID: 26229141]
[13]
Jack CR Jr, Knopman DS, Jagust WJ, et al. Hypothetical model of dynamic biomarkers of the Alzheimer’s pathological cascade. Lancet Neurol 2010; 9(1): 119-28.
[http://dx.doi.org/10.1016/S1474-4422(09)70299-6] [PMID: 20083042]
[14]
Jennings D, Siderowf A, Stern M, et al. Imaging prodromal Parkinson disease: the Parkinson associated risk syndrome study. Neurology 2014; 83(19): 1739-46.
[http://dx.doi.org/10.1212/WNL.0000000000000960] [PMID: 25298306]
[15]
Mahlknecht P, Seppi K, Poewe W. The concept of prodromal Parkinson’s disease. J Parkinsons Dis 2015; 5(4): 681-97.
[http://dx.doi.org/10.3233/JPD-150685] [PMID: 26485429]
[16]
Mirpour S, Turkbey EB, Marashdeh W, El Khouli R, Subramaniam RM. Impact of DAT-SPECT on management of patients suspected of Parkinsonism. Clin Nucl Med 2018; 43(10): 710-4.
[http://dx.doi.org/10.1097/RLU.0000000000002240] [PMID: 30153144]
[17]
Brooks DJ, Pavese N. Imaging biomarkers in Parkinson’s disease. Prog Neurobiol 2011; 95(4): 614-28.
[http://dx.doi.org/10.1016/j.pneurobio.2011.08.009] [PMID: 21896306]
[18]
Palumbo B, Fravolini ML, Nuvoli S, et al. Comparison of two neural network classifiers in the differential diagnosis of essential tremor and Parkinson’s disease by (123)I-FP-CIT brain SPECT. Eur J Nucl Med Mol Imaging 2010; 37(11): 2146-53.
[http://dx.doi.org/10.1007/s00259-010-1481-6] [PMID: 20567820]
[19]
Berardelli A, Wenning GK, Antonini A, et al. EFNS/MDS-ES/ENS [corrected] recommendations for the diagnosis of Parkinson’s disease. Eur J Neurol 2013; 20(1): 16-34.
[http://dx.doi.org/10.1111/ene.12022] [PMID: 23279440]
[20]
Nuvoli S, Palumbo B, Malaspina S, Madeddu G, Spanu A. 123I-ioflupane SPET and 123I-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 2018; 21(1): 60-8.
[PMID: 29550847]
[21]
McKeith IG, Boeve BF, Dickson DW, et al. Diagnosis and management of dementia with Lewy bodies: Fourth consensus report of the DLB Consortium. Neurology 2017; 89(1): 88-100.
[http://dx.doi.org/10.1212/WNL.0000000000004058] [PMID: 28592453]
[22]
McKeith I, O’Brien J, Walker Z, et al. Sensitivity and specificity of dopamine transporter imaging with 123I-FP-CIT SPECT in dementia with Lewy bodies: A phase III, multicentre study. Lancet Neurol 2007; 6(4): 305-13.
[http://dx.doi.org/10.1016/S1474-4422(07)70057-1] [PMID: 17362834]
[23]
Isaacson SH, Fisher S, Gupta F, et al. Clinical utility of DaTscan™ imaging in the evaluation of patients with parkinsonism: A US perspective. Expert Rev Neurother 2017; 17(3): 219-25.
[http://dx.doi.org/10.1080/14737175.2017.1256205] [PMID: 27813429]
[24]
Pirker W, Asenbaum S, Bencsits G, et al. [123I]beta-CIT SPECT in multiple system atrophy, progressive supranuclear palsy, and corticobasal degeneration. Mov Disord 2000; 15(6): 1158-67.
[http://dx.doi.org/10.1002/1531-8257(200011)15:6<1158::AID-MDS1015>3.0.CO;2-0] [PMID: 11104200]
[25]
Cummings JL, Henchcliffe C, Schaier S, Simuni T, Waxman A, Kemp P. The role of dopaminergic imaging in patients with symptoms of dopaminergic system neurodegeneration. Brain 2011; 134(Pt 11): 3146-66.
[http://dx.doi.org/10.1093/brain/awr177] [PMID: 21810889]
[26]
Walker Z, Gandolfo F, Orini S, et al. Clinical utility of FDG PET in Parkinson’s disease and atypical parkinsonism associated with dementia. Eur J Nucl Med Mol Imaging 2018; 45(9): 1534-45.
[http://dx.doi.org/10.1007/s00259-018-4031-2] [PMID: 29779045]
[27]
Meyer PT, Frings L, Rücker G, Hellwig S. 18F-FDG PET in Parkinsonism: differential diagnosis and evaluation of cognitive impairment. J Nucl Med 2017; 58(12): 1888-98.
[http://dx.doi.org/10.2967/jnumed.116.186403] [PMID: 28912150]
[28]
Darcourt J, Booij J, Tatsch K, et al. EANM procedure guidelines for brain neurotransmission SPECT using (123)I-labelled dopamine transporter ligands, version 2. Eur J Nucl Med Mol Imaging 2010; 37(2): 443-50.
[http://dx.doi.org/10.1007/s00259-009-1267-x] [PMID: 19838702]
[29]
Nuvoli S, Spanu A, Piras MR, et al. 123I-ioflupane brain SPECT and 123I-MIBG cardiac planar scintigraphy combined use in uncertain parkinsonian disorders. Medicine (Baltimore) 2017; 96(21): e6967.
[http://dx.doi.org/10.1097/MD.0000000000006967] [PMID: 28538394]
[30]
Roberts G, Lloyd JJ, Petrides GS, et al. 123I-FP-CIT striatal binding ratios do not decrease significantly with age in older adults. Ann Nucl Med 2019; 33(6): 434-43.
[http://dx.doi.org/10.1007/s12149-019-01352-x] [PMID: 30900103]
[31]
Sabri O, Ringelstein EB, Hellwig D, et al. Neuropsychological impairment correlates with hypoperfusion and hypometabolism but not with severity of white matter lesions on MRI in patients with cerebral microangiopathy. Stroke 1999; 30(3): 556-66.
[http://dx.doi.org/10.1161/01.STR.30.3.556] [PMID: 10066852]
[32]
Frantellizzi V, Pani A, Ricci M, Locuratolo N, Fattapposta F, De Vincentis G. Neuroimaging in vascular cognitive impairment and dementia: A systematic review. J Alzheimers Dis 2020; 73(4): 1279-94.
[http://dx.doi.org/10.3233/JAD-191046] [PMID: 31929166]
[33]
Varrone A, Asenbaum S, Vander Borght T, et al. EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2. Eur J Nucl Med Mol Imaging 2009; 36(12): 2103-10.
[http://dx.doi.org/10.1007/s00259-009-1264-0] [PMID: 19838705]
[34]
Kovacs GG. Concepts and classification of neurodegenerative diseases. Handb Clin Neurol 2017; 145: 301-7.
[http://dx.doi.org/10.1016/B978-0-12-802395-2.00021-3] [PMID: 28987178]
[35]
Buchert R, Buhmann C, Apostolova I, Meyer PT, Gallinat J. Nuclear imaging in the diagnosis of clinically uncertain Parkinsonian syndromes. Dtsch Arztebl Int 2019; 116(44): 747-54.
[http://dx.doi.org/10.3238/arztebl.2019.0747] [PMID: 31774054]
[36]
Nuvoli S, Spanu A, Madeddu G. Brain SPECT with perfusion radiopharmaceuticals and dopaminergic system radiocompounds in dementia disorders. Curr Alzheimer Res 2017; 14(2): 143-53.
[http://dx.doi.org/10.2174/1567205013666161019144406] [PMID: 27774875]
[37]
Nuvoli S, Spanu A, Fravolini ML, et al. [123I]Metaiodobenzylguanidine (MIBG) Cardiac Scintigraphy and Automated Classification Techniques in Parkinsonian Disorders. Mol Imaging Biol 2020; 22(3): 703-10.
[http://dx.doi.org/10.1007/s11307-019-01406-6] [PMID: 31309370]
[38]
Nicastro N, Garibotto V, Burkhard PR. The role of molecular imaging in assessing degenerative parkinsonism -an updated review. Swiss Med Wkly 2018; 26 148:w14621 eCollection 2018
[39]
Pagano G, Niccolini F, Politis M. Imaging in Parkinson’s disease. Clin Med (Lond) 2016; 16(4): 371-5.
[http://dx.doi.org/10.7861/clinmedicine.16-4-371] [PMID: 27481384]
[40]
Tang J, Yang B, Adams MP, et al. Artificial neural network-based prediction of outcome in Parkinson’s disease patients using DaTscan SPECT imaging features. Mol Imaging Biol 2019; 21(6): 1165-73.
[http://dx.doi.org/10.1007/s11307-019-01334-5] [PMID: 30847821]
[41]
Eckert T, Barnes A, Dhawan V, et al. FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage 2005; 26(3): 912-21.
[http://dx.doi.org/10.1016/j.neuroimage.2005.03.012] [PMID: 15955501]
[42]
Mäkinen E, Joutsa J, Johansson J, Mäki M, Seppänen M, Kaasinen V. Visual versus automated analysis of [I-123]FP-CIT SPECT scans in parkinsonism. J Neural Transm (Vienna) 2016; 123(11): 1309-18.
[http://dx.doi.org/10.1007/s00702-016-1586-6] [PMID: 27324804]
[43]
Filippi L, Manni C, Pierantozzi M, et al. 123I-FP-CIT semi-quantitative SPECT detects preclinical bilateral dopaminergic deficit in early Parkinson’s disease with unilateral symptoms. Nucl Med Commun 2005; 26(5): 421-6.
[http://dx.doi.org/10.1097/00006231-200505000-00005] [PMID: 15838424]
[44]
Kato T, Inui Y, Nakamura A, Ito K. Brain fluorodeoxyglucose (FDG) PET in dementia. Ageing Res Rev 2016; 30: 73-84.
[http://dx.doi.org/10.1016/j.arr.2016.02.003] [PMID: 26876244]
[45]
Lehman VT, Carter RE, Claassen DO, et al. Visual assessment versus quantitative three-dimensional stereotactic surface projection fluorodeoxyglucose positron emission tomography for detection of mild cognitive impairment and Alzheimer disease. Clin Nucl Med 2012; 37(8): 721-6.
[http://dx.doi.org/10.1097/RLU.0b013e3182478d89] [PMID: 22785496]
[46]
Garibotto V, Montandon ML, Viaud CT, et al. Regions of interest-based discriminant analysis of DaTSCAN SPECT and FDG-PET for the classification of dementia. Clin Nucl Med 2013; 38(3): e112-7.
[http://dx.doi.org/10.1097/RLU.0b013e318279b991] [PMID: 23357822]
[47]
Jolepalem P, Balon HR, Wong CY, Wu D. Complementary role of 18F-FDG PET and 123I-ioflupane SPECT in the diagnosis of Lewy body disease. J Nucl Med Technol 2014; 42(3): 233-4.
[http://dx.doi.org/10.2967/jnmt.113.133199] [PMID: 25033885]
[48]
Lim SM, Katsifis A, Villemagne VL, et al. The 18F-FDG PET cingulate island sign and comparison to 123I-beta-CIT SPECT for diagnosis of dementia with Lewy bodies. J Nucl Med 2009; 50(10): 1638-45.
[http://dx.doi.org/10.2967/jnumed.109.065870] [PMID: 19759102]
[49]
Jellinger KA, Seppi K, Wenning GK, Poewe W. Impact of coexistent Alzheimer pathology on the natural history of Parkinson’s disease. J Neural Transm (Vienna) 2002; 109(3): 329-39.
[http://dx.doi.org/10.1007/s007020200027] [PMID: 11956955]
[50]
Li X, James S, Lei P. Interactions between α-synuclein and tau protein: Implications to neurodegenerative disorders. J Mol Neurosci 2016; 60(3): 298-304.
[http://dx.doi.org/10.1007/s12031-016-0829-1] [PMID: 27629562]
[51]
Armstrong RA, Lantos PL, Cairns NJ. Overlap between neurodegenerative disorders. Neuropathology 2005; 25(2): 111-24.
[http://dx.doi.org/10.1111/j.1440-1789.2005.00605.x] [PMID: 15875904]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 18
ISSUE: 3
Year: 2021
Published on: 23 September, 2021
Page: [196 - 207]
Pages: 12
DOI: 10.2174/1567205018666210608112302
Price: $65

Article Metrics

PDF: 99
HTML: 3