PET and SPECT in the assessment of monoaminergic brain systems in extrapyramidal disorders

Cover Page


Cite item

Full Text

Abstract

In clinical neurology, biomarkers of central neurotransmitter imbalance have been of particular interest in the study of motor disorders and examination of patients with Parkinson’s disease (PD) and other extrapyramidal diseases, primarily to assess the exchange of dopamine and other monoamines in the brain. Radioisotope visualization methods, such as positron emission tomography (PET) and single-photon emission computed tomography (SPECT) with the corresponding radiopharmaceuticals, are the most informative for these purposes. This article presents a comparative analysis of the wide range of existing ligands and molecular targets for functional neuroimaging using radioisotopes of the nigrostriatal system and the other monoaminergic systems of the brain, with emphasis on the study of the dopamine transporter, dopamine receptors and dopamine-metabolysing enzymes. The modern possibilities of PET and SPECT for the early diagnosis of PD, and the differential diagnosis of this disease with clinically similar syndromes (dystonia, atypical and drug-induced parkinsonism, essential tremor), as well as for monitoring the pathological process and assessing the results of various therapeutic interventions are evaluated. The role of functional neuroimaging in the objective assessment in vivo of the non-motor symptoms of PD, such as depression, impulse control disorders, pathological fatigue and orthostatic hypotension, is emphasized.

About the authors

Marianna V. Selikhova

Southmead Hospital

Author for correspondence.
Email: m.selikhova@talk21.com
Великобритания, Bristol

Elena A. Katunina

N.I. Pirogov Russian National Research Medical University

Email: m.selikhova@talk21.com
Россия, Moscow

Alan Whone

Southmead Hospital

Email: m.selikhova@talk21.com
Великобритания, Bristol

References

  1. Illarioshkin S.N. [Early (dodement) forms of cognitive disorders]. Consilium Medicum 2007; 9(2): 107−111. (In Russ.)
  2. Illarioshkin S.N., Vlassenko A.G., Fedotova E.Yu. [Current means for identifying the latent stage of a neurodegenerative process]. Annals of clinical and experimental neurology 2013; 7(2): 39–50. (In Russ.)
  3. Zagorovskaya T.B., Illarioshkin S.N., Slominsky P.A. et al. [Clinical and genetic analysis of juvenile parkinsonism in Russia]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova 2004; 104(8): 66–72. (In Russ.)
  4. Illarioshkin S.N. [The course of Parkinson's disease and approaches to early diagnosis]. In: Illarioshkin S.N., Levin O.S. (eds.) [Parkinson's disease and movement disorders. A guide for doctors]. Moscow, 2011: 41–47. (In Russ.)
  5. Benamer H.T., Oertel W.H., Patterson J. et al. Prospective study of presynaptic dopaminergic imaging in patients with mild parkinsonism and tremor disorders part 1: Baseline and 3-month observations. Mov Disord 2003; 18: 977–984. doi: 10.1002/mds.10482. PMID: 14502664.
  6. Leenders K.L., Salmon E.P., Tyrrell P. et al. The nigrostriatal dopaminergic system assessed in vivo by positron emission tomography in healthy volunteer subjects and patients with Parkinson's disease. Arch Neurol 1990; 47: 1290–1298. PMID: 2123623.
  7. Piccini P., Whone A. Functional brain imaging in the differential diagnosis of Parkinson's disease. Lancet Neurol 2004; 3: 284–290. doi: 10.1016/S1474-4422(04)00736-7. PMID: 15099543.
  8. Levin O.S., Fedorova N.V., Shtok V.N. [Differential diagnosis of parkinsonism]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova 2003; 2: 54–60. (In Russ.)
  9. Brooks D.J., Playford E.D., Ibanez V. et al. Isolated tremor and disruption of the nigrostriatal dopaminergic system: an 18F-dopa PET study. Neurology 1992; 42: 1554–1560. PMID: 1641153.
  10. Golubev V.L., Levin Ya.I., Vein A.M. [Parkinson's disease and Parkinson's syndrome]. Moscow, 1999. (In Russ.)
  11. Fahn S., Oakes D., Shoulson I. et al. Levodopa and the progression of Parkinson’s disease. N Engl J Med 2004; 351: 2498–2508. doi: 10.1056/NEJMoa033447. PMID: 15590952.
  12. Hughes A.J., Daniel S.E., Lees A.J. Improved accuracy of clinical diagnosis of Lewy body Parkinson's disease. Neurology 2001; 57: 1497–1499. PMID: 11673599.
  13. de Natale E.R., Niccolini F., Wilson H., Politis M. Molecular imaging of the dopaminergic system in idiopathic Parkinson's disease. Int Rev Neurobiol 2018; 141: 131–172. doi: 10.1016/bs.irn.2018.08.003. PMID: 30314595.
  14. Whone A.L., Bailey D.L., Remy P. et al. A technique for standardised central analysis of 6-[18F]-fluoro-L-dopa PET data from a multicenter study. J Nucl Med 2004; 45: 1135–1145. PMID: 15235059.
  15. Garnett E.S., Firnau G., Nahmias C. Dopamine visualized in the basal ganglia of living man. Nature 1983; 305: 137–138. PMID: 6604227.
  16. Moore R.Y., Whone A.L., McGowan S., Brooks D.J. Monoamine neuron innervation of the normal human brain: an 18F-DOPA PET study. Brain Res 2003; 982: 137–145. PMID: 12915249.
  17. Otsuka M., Ichiya Y., Kuwabara Y. et al. Differences in the reduced 18F-Dopa uptakes of the caudate and the putamen in Parkinson's disease: correlations with the three main symptoms. J Neurol Sci 1996; 136: 169–173. PMID: 8815166.
  18. Morrish P.K., Sawle G.V., Brooks D.J. Clinical and [18F]dopa PET findings in early Parkinson's disease. J Neurol Neurosurg Psychiatry 1995; 59: 597–600. PMID: 7500096.
  19. Benamer H.T., Patterson J., Wyper D.J. et al. Correlation of Parkinson's disease severity and duration with [123I]-FP-CIT SPECT striatal uptake. Mov Disord 2000; 15: 692–698. doi: 10.1002/mds.10482. PMID: 14502664.
  20. Brooks D.J. Morphological and functional imaging studies on the diagnosis and progression of Parkinson's disease. J Neurol 2000; 247: II11–II18. PMID: 10991656.
  21. Brück A., Aalto S., Rauhala E. et al. A follow-up study on 6-[18F]fluoro-L-dopa uptake in early Parkinson's disease shows nonlinear progression in the putamen. Mov Disord 2009; 24: 1009–1015. doi: 10.1002/mds.22484. PMID: 19260097.
  22. Snow B.J., Tooyama I., McGeer E.G. et al. Human positron emission tomographic [18F] fluorodopa studies correlate with dopamine cell counts and levels. Ann Neurol 1993; 34: 324–330. doi: 10.1002/ana.410340304. PMID: 8363349.
  23. Whone A.L., Watts R.L., Stoessl A.J. et al. REAL-PET Study Group Slower progression of Parkinson's disease with ropinirole versus levodopa: the REAL-PET study. Ann Neurol 2003; 54: 93–101. doi: 10.1002/ana.10609. PMID: 12838524.
  24. Morrish P.K., Rakshi J.S., Bailey D.L. et al. Measuring the rate of progression and estimating the preclinical period of Parkinson's disease with [18F]dopa PET. J Neurol Neurosurg Psychiatry 1998; 64: 314–319. PMID: 9527140.
  25. Fahn S., Elton R.L., Members of the UPDRS Development Committee. Unified Parkinson's disease rating scale. In: Fahn S., Marsden C.D., Calne D.B., Goldstein M. (eds). Recent developments in Parkinson's disease. N.J., 1987: 153–163.
  26. Vingerhoets F.J., Snow B.J., Lee C.S. et al. Longitudinal fluorodopa positron emission tomographic studies of the evolution of idiopathic parkinsonism. Ann Neurol 1994; 36: 759–764. doi: 10.1002/ana.410360512. PMID: 7979222.
  27. Piccini P., Burn D.J., Ceravolo R. et al. The role of inheritance in sporadic Parkinson's disease: evidence from a longitudinal study of dopaminergic function in twins. Ann Neurol 1999; 45: 577–582. PMID: 10319879.
  28. Wenning G.K., Odin P., Morrish P. et al. Short- and long-term survival and function of unilateral intrastriatal dopaminergic grafts in Parkinson's disease. Ann Neurol 1997; 42: 95–107. doi: 10.1002/ana.410420115. PMID: 9225690.
  29. Hagell P., Piccini P., Björklund A. et al. Dyskinesias following neural transplantation in Parkinson's disease. Nat Neurosci 2002; 5: 627–628 doi: 10.1038/nn863. PMID: 12042822.
  30. Lang A.E., Langston J.W., Stoessl A.J. et al. GDNF in treatment of Parkinson's disease: response to editorial. Lancet Neurol 2006; 5: 200–202. PMID: 16488373. doi: 10.1016/S1474-4422(06)70359-3.
  31. Whone A., Luz M., Boca M. et al. Randomized trial of intermittent intraputamenal glial cell line-derived neurotrophic factor in Parkinson’s disease. Brain 2019; 142: 512–525. doi: 10.1093/brain/awz023. PMID: 30808022.
  32. Pavese N., Rivero-Bosch M., Lewis S.J. et al. Progression of monoaminergic dysfunction in Parkinson's disease: a longitudinal 18F-dopa PET study. Neuroimage 2011; 56: 1463–1468. doi: 10.1016/j.neuroimage.2011.03.012. PMID: 21396455.
  33. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991; 114: 2283–2301. PMID: 1933245.
  34. Burn D.J., Sawle G.V., Brooks D.J. Differential diagnosis of Parkinson's disease, multiple system atrophy, and Steele-Richardson-Olszewski syndrome: discriminant analysis of striatal 18F-dopa PET data. J Neurol Neurosurg Psychiatry 1994; 57: 278–284. PMID: 8158173.
  35. Brooks D.J., Ibanez V., Sawle G.V. et al. Striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11C-raclopride and positron emission tomography. Ann Neurol 1992; 31: 184–192. doi: 10.1002/ana.410310209. PMID: 1575457.
  36. Stoessl A.J. Positron emission tomography in premotor Parkinson's disease. Parkinsonism Relat Disord 2007; 13(Suppl. 3): S421–S424. doi: 10.1016/S1353-8020(08)70041-5. PMID: 18267275.
  37. Lee C.S., Samii A., Sossi V. et al. In vivo positron emission tomographic evidence for compensatory changes in presynaptic dopaminergic nerve terminals in Parkinson's disease. Ann Neurol 2000; 47: 493–503. PMID: 10762161.
  38. Loane C., Politis M. Positron emission tomography neuroimaging in Parkinson’s disease. Am J Transl Res 2011; 3: 323–341. PMID: 21904653.
  39. Schwarz J., Tatsch K., Arnold G. et al. 123I-iodobenzamide-SPECT in 83 patients with de novo parkinsonism. Neurology 1993; 43: S17–S20. PMID: 8264906.
  40. Brooks D.J. Molecular imaging of dopamine transporters. Ageing Res Rev 2016; 30: 114–121. doi: 10.1016/j.arr.2015.12.009. PMID: 26802555.
  41. Seibyl J.P., Marek K.L., Quinlan D. et al. Decreased single-photon emission computed tomographic [123I] beta-CIT striatal uptake correlates with symptom severity in Parkinson's disease. Ann Neurol 1995; 38: 589–598. doi: 10.1002/ana.410380407. PMID: 7574455.
  42. Kim Y.J., Ichise M., Ballinger J.R. et al. Combination of dopamine transporter and D2 receptor SPECT in the diagnostic evaluation of PD, MSA, and PSP. Mov Disord 2002; 17: 303–312. PMID: 11921116.
  43. Kish S.J., Tong J., Hornykiewicz O. et al. Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 2008; 131: 120–131. PMID: 17956909. doi: 10.1093/brain/awm239.
  44. Asenbaum S., Pirker W., Angelberger P. et al. [123I]beta-CIT and SPECT in essential tremor and Parkinson's disease. J Neural Transm (Vienna) 1998; 105: 1213–1228. doi: 10.1007/s007020050124. PMID: 9928890.
  45. Brücke T., Djamshidian S., Bencsits G. et al. SPECT and PET imaging of the dopaminergic system in Parkinson's disease. J Neurol 2000; 247: IV/2–IV/7. PMID: 11199811.
  46. Silveira-Moriyama L., Schwingenschuh P., O'Donnell A. et al. Olfaction in patients with suspected parkinsonism and scans without evidence of dopaminergic deficit (SWEDDs). J Neurol Neurosurg Psychiatry 2009; 80: 744–748. doi: 10.1136/jnnp.2009.172825. PMID: 19276101.
  47. Marshall V., Grosset D. Role of dopamine transporter imaging in routine clinical practice. Mov Disord 2003; 18: 1415–1423. doi: 10.1002/mds.10592. PMID: 14673877.
  48. Marshall V.L., Patterson J., Hadley D.M. et al. Successful antiparkinsonian medication withdrawal in patients with parkinsonism and normal FP-CIT SPECT. Mov Disord 2006; 21: 2247–2250. doi: 10.1002/mds.21159. PMID: 17078059.
  49. Lorberboym M., Treves T.A., Melamed E. et al. [123I]-FP/CIT SPECT imaging for distinguishing drug-induced parkinsonism from Parkinson’s disease. Mov Disord 2006; 21: 510–514. doi: 10.1002/mds.20748. PMID: 16250023.
  50. Plotkin M., Amthauer H., Klaffke S. et al. Combined 123I-FP-CIT and 123I-IBZM SPECT for the diagnosis of parkinsonian syndromes: study on 72 patients. J Neural Transm (Vienna) 2005; 112: 677–692. doi: 10.1007/s00702-004-0208-x. PMID: 15375677.
  51. Noyce A.J., Lees A.J., Schrag A.E. The prediagnostic phase of Parkinson's disease. J Neurol Neurosurg Psychiatry 2016; 87: 871–878. doi: 10.1136/jnnp-2015-311890. PMID: 26848171.
  52. Parkinson Study Group. Pramipexole vs levodopa as initial treatment for Parkinson disease: A randomized controlled trial. JAMA 2000; 284: 1931–1938. PMID: 11035889.
  53. Piccini P., Morrish P.K., Turjanski N. et al. Dopaminergic function in familial Parkinson's disease: a clinical and 18F-dopa positron emission tomography study. Ann Neurol 1997; 41: 222–229. doi: 10.1002/ana.410410213. PMID: 9029071.
  54. Adams J.R., van Netten H., Schulzer M. et al. PET in LRRK2 mutations: comparison to sporadic Parkinson's disease and evidence for presymptomatic compensation. Brain 2005; 128: 2777–2785. doi: 10.1093/brain/awh607. PMID: 16081470.
  55. Khan N.L., Brooks D.J., Pavese N. et al. Progression of nigrostriatal dysfunction in a parkin kindred: an [18F]dopa PET and clinical study. Brain 2002; 125: 2248–2256. PMID: 12244082.
  56. Hilker R., Razai N., Ghaemi M. et al. [18F] fluorodopa uptake in the upper brainstem measured with positron emission tomography correlates with decreased REM sleep duration in early Parkinson's disease. Clin Neurol Neurosurg 2003; 105: 262–269. PMID: 12954543.
  57. Rinne J.O., Laihinen A., Ruottinen H. et al. Increased density of dopamine D2 receptors in the putamen, but not in the caudate nucleus in early Parkinson's disease: a PET study with [11C] raclopride. J Neurol Sci 1995; 132: 156–161. PMID: 8543941.
  58. Antonini A., Schwarz J., Oertel W.H. et al. Long-term changes of striatal dopamine D2 receptors in patients with Parkinson's disease: a study with positron emission tomography and [11C] raclopride. Mov Disord 1997; 12: 33–38. doi: 10.1002/mds.870120107. PMID: 8990051.
  59. Antonini A., Leenders K.L., Vontobel P. et al. Complementary PET studies of striatal neuronal function in the differential diagnosis between multiple system atrophy and Parkinson's disease. Brain 1997; 120: 2187–2195. PMID: 9448574.
  60. Evans A.H., Pavese N., Lawrence A.D. et al. Compulsive drug use linked to sensitized ventral striatal dopamine transmission. Ann Neurol 2006; 59: 852–858. doi: 10.1002/ana.20822. PMID: 16557571.
  61. O'Sullivan S.S., Wu K., Politis M. et al. Cue-induced striatal dopamine release in Parkinson's disease-associated impulsive-compulsive behaviours. Brain 2011; 134: 969–978. doi: 10.1093/brain/awr003. PMID: 21349901.
  62. Steeves T.D., Miyasaki J., Zurowski M. et al. Increased striatal dopamine release in Parkinsonian patients with pathological gambling: a [11C] raclopride PET study. Brain 2009; 132: 1376–1385. doi: 10.1093/brain/awp054. PMID: 19346328.
  63. Maeda T., Nagata K., Yoshida Y., Kannari K. Serotonergic hyperinnervation into the dopaminergic denervated striatum compensates for dopamine conversion from exogenously administered L-DOPA. Brain Res 2005; 1046: 230–233. doi: 10.1016/j.brainres.2005.04.019. PMID: 15894297.
  64. Politis M., Loane C. Serotonergic dysfunction in Parkinson's disease and its relevance to disability. ScientificWorldJournal 2011; 11: 1726–1734. doi: 10.1100/2011/172893. PMID: 22125431.
  65. Stoessl A.J. Functional imaging studies of non-motoric manifestations of Parkinson's disease. Parkinsonism Relat Disord 2009; 15: S13–S16. doi: 10.1016/S1353-8020(09)70771-0. PMID: 20082973.
  66. Doder M., Rabiner E.A., Turjanski N. et al. Brain serotonin HT1A receptors in Parkinson’s disease with and without depression measured by positron emission tomography and 11C-WAY100635. Mov Disord 2000; 15 (Suppl 3): 213.
  67. Politis M., Wu K., Loane C. et al. Depressive symptoms in PD correlate with higher 5-HTT binding in raphe and limbic structures. Neurology 2010; 75: 1920–1927. PMID: 21098407. doi: 10.1212/WNL.0b013e3181feb2ab.
  68. Remy P., Doder M., Lees A.J. et al. Depression in Parkinson's disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 2005; 128: 1314–1322. doi: 10.1093/brain/awh445. PMID: 15716302.
  69. Joers V., Emborg M.E. Modeling and imaging cardiac sympathetic neurodegeneration in Parkinson’s disease. Am J Nucl Med Mol Imaging 2014; 4: 125–159. PMID: 24753981.
  70. Wong K.K., Raffel D.M., Koeppe R.A. et al. Pattern of cardiac sympathetic denervation in idiopathic Parkinson disease studied with 11C hydroxyephedrine PET. Radiology 2012; 265: 240–247. doi: 10.1148/radiol.12112723. PMID: 22843766.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2019 Selikhova M.V., Katunina E.A., Whone A...

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77-83204 от 12.05.2022.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies