Imaging Biomarkers in Prodromal and Earliest Phases of Parkinson's Disease
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, přehledy
PubMed
38339941
PubMed Central
PMC11492013
DOI
10.3233/jpd-230385
PII: JPD230385
Knihovny.cz E-zdroje
- Klíčová slova
- MRI, PET, Parkinson’s disease, biomarker, diagnosis, neuroimaging, prodromal, progression,
- MeSH
- biologické markery * metabolismus analýza MeSH
- lidé MeSH
- magnetická rezonanční tomografie MeSH
- neurozobrazování metody MeSH
- optická koherentní tomografie metody MeSH
- Parkinsonova nemoc * diagnostické zobrazování metabolismus diagnóza MeSH
- pozitronová emisní tomografie MeSH
- prodromální symptomy * MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- biologické markery * MeSH
Assessing imaging biomarker in the prodromal and early phases of Parkinson's disease (PD) is of great importance to ensure an early and safe diagnosis. In the last decades, imaging modalities advanced and are now able to assess many different aspects of neurodegeneration in PD. MRI sequences can measure iron content or neuromelanin. Apart from SPECT imaging with Ioflupane, more specific PET tracers to assess degeneration of the dopaminergic system are available. Furthermore, metabolic PET patterns can be used to anticipate a phenoconversion from prodromal PD to manifest PD. In this regard, it is worth mentioning that PET imaging of inflammation will gain significance. Molecular imaging of neurotransmitters like serotonin, noradrenaline and acetylcholine shed more light on non-motor symptoms. Outside of the brain, molecular imaging of the heart and gut is used to measure PD-related degeneration of the autonomous nervous system. Moreover, optical coherence tomography can noninvasively detect degeneration of retinal fibers as a potential biomarker in PD. In this review, we describe these state-of-the-art imaging modalities in early and prodromal PD and point out in how far these techniques can and will be used in the future to pave the way towards a biomarker-based staging of PD.
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van Eimeren T, Antonini A, Berg D, Bohnen N, Ceravolo R, Drzezga A, Höglinger GU, Higuchi M, Lehericy S, Lewis S, Monchi O, Nestor P, Ondrus M, Pavese N, Peralta MC, Piccini P, Pineda-Pardo JÁ, Rektorová I, Rodríguez-Oroz M, Rominger A, Seppi K, Stoessl AJ, Tessitore A, Thobois S, Kaasinen V, Wenning G, Siebner HR, Strafella AP, Rowe JB (2019) Neuroimaging biomarkers for clinicaltrials in atypical parkinsonian disorders: Proposal for aNeuroimaging Biomarker Utility System. Alzheimers Dement(Amst) 11, 301–309. PubMed PMC
Simuni T, Chahine LM, Poston K, Brumm M, Buracchio T, Campbell M, Chowdhury S, Coffey C, Concha-Marambio L, Dam T, DiBiaso P, Foroud T, Frasier M, Gochanour C, Jennings D, Kieburtz K, Kopil CM, Merchant K, Mollenhauer B, Montine T, Nudelman K, Pagano G, Seibyl J, Sherer T, Singleton A, Stephenson D, Stern M, Soto C, Tanner CM, Tolosa E, Weintraub D, Xiao Y, Siderowf A, Dunn B, Marek K (2024). A biological definition of neuronal α-synuclein disease: towards an integrated staging system for research. Lancet Neural 23, 178–190. PubMed
Höglinger GU, Adler CH, Berg D, Klein C, Outeiro TF, Poewe W, Postuma R, Stoessl AJ, Lang AE (2024) A biological classification of Parkinson’s disease: the Syn-NeurGe research diagnostic criteria. Lancet Neural 23, 191–204. PubMed
Krajcovicova L, Klobusiakova P, Rektorova I (2019) Gray matter changes in Parkinson’s and Alzheimer’s disease and relation to cognition. Curr Neurol Neurosci Rep 19, 85. PubMed PMC
Banwinkler M, Dzialas V, Parkinson’s Progression Markers Initiative, Hoenig MC, van Eimeren T (2022) Gray matter volume loss in proposed brain-first and body-first Parkinson’s disease subtypes. Mov Disord 37, 2066–2074. PubMed
Rektorova I, Biundo R, Marecek R, Weis L, Aarsland D, Antonini A (2014) Grey matter changes in cognitively impaired Parkinson’s disease patients. PLoS One 9, e85595. PubMed PMC
Zeighami Y, Fereshtehnejad S-M, Dadar M, Collins DL, Postuma RB, Misić B, Dagher A (2019) A clinical-anatomical signature ofParkinson’s disease identified with partial least squares andmagnetic resonance imaging. Neuroimage 190, 69–78. PubMed
Fereshtehnejad S-M, Zeighami Y, Dagher A, Postuma RB (2017) Clinical criteria for subtyping Parkinson’s disease: Biomarkers and longitudinal progression. Brain 140, 1959–1976. PubMed
Rahayel S, Postuma RB, Montplaisir J, Misić B, Tremblay C, Vo A, Lewis S, Matar E, Ehgoetz Martens K, Blanc F, Yao C, Carrier J, Monchi O, Gaubert M, Dagher A, Gagnon J-F (2021) A prodromalbrain-clinical pattern of cognition in synucleinopathies. AnnNeurol 89, 341–357. PubMed
Yau Y, Zeighami Y, Baker TE, Larcher K, Vainik U, Dadar M, Fonov VS, Hagmann P, Griffa A, Misić B, Collins DL, Dagher A (2018) Network connectivity determines cortical thinning in earlyParkinson’s disease progression. Nat Commun 9, 12. PubMed PMC
Atkinson-Clement C, Pinto S, Eusebio A, Coulon O (2017) Diffusion tensor imaging in Parkinson’s disease: Review and meta-analysis. Neuroimage Clin 16, 98–110. PubMed PMC
Schwarz ST, Abaei M, Gontu V, Morgan PS, Bajaj N, Auer DP (2013) Diffusion tensor imaging of nigral degeneration in Parkinson’s disease: A region-of-interest and voxel-based study at 3 T and systematic review with meta-analysis. Neuroimage Clin 3, 481–488. PubMed PMC
Khairnar A, Ruda-Kucerova J, Szabó N, Drazanova E, Arab A, Hutter-Paier B, Neddens J, Latta P, Starcuk Z, Rektorova I (2017) Early and progressive microstructural brain changes in mice overexpressing human α-synuclein detected by diffusion kurtosis imaging. Brain Behav Immun 61, 197–208. PubMed
Sejnoha Minsterova A, Klobusiakova P, Pies A, Galaz Z, Mekyska J, Novakova L, Nemcova Elfmarkova N, Rektorova I (2020) Patterns of diffusion kurtosis changes in Parkinson’s disease subtypes. Parkinsonism Relat Disord 81, 96–102. PubMed
Zhou L, Li G, Zhang Y, Zhang M, Chen Z, Zhang L, Wang X, Zhang M, Ye G, Li Y, Chen S, Li B, Wei H, Liu J (2021) Increased free water in the substantia nigra in idiopathic REM sleep behaviour disorder. Brain 144, 1488–1497. PubMed
Ofori E, Pasternak O, Planetta PJ, Burciu R, Snyder A, Febo M, Golde TE, Okun MS, Vaillancourt DE (2015) Increased free water in the substantia nigra of Parkinson’s disease: A single-site and multi-site study. Neurobiol Aging 36, 1097–1104. PubMed PMC
Barber TR, Klein JC, Mackay CE, Hu MTM (2017) Neuroimaging in pre-motor Parkinson’s disease. Neuroimage Clin 15, 215–227. PubMed PMC
De Marzi R, Seppi K, Högl B, Müller C, Scherfler C, Stefani A, Iranzo A, Tolosa E, Santamarìa J, Gizewski E, Schocke M, Skalla E, Kremser C, Poewe W (2016) Loss of dorsolateral nigralhyperintensity on 3.0 tesla susceptibility-weighted imaging inidiopathic rapid eye movement sleep behavior disorder. AnnNeurol 79, 1026–1030. PubMed
Sun H, Walsh AJ, Lebel RM, Blevins G, Catz I, Lu J-Q, Johnson ES, Emery DJ, Warren KG, Wilman AH (2015) Validation of quantitative susceptibility mapping with Perls’ iron staining for subcortical gray matter. Neuroimage 105, 486–492. PubMed
Prange S, Metereau E, Thobois S (2019) Structural imaging in Parkinson’s disease: New developments. Curr Neurol Neurosci Rep 19, 50. PubMed
Biondetti E, Santin MD, Valabrègue R, Mangone G, Gaurav R, Pyatigorskaya N, Hutchison M, Yahia-Cherif L, Villain N, Habert M-O, Arnulf I, Leu-Semenescu S, Dodet P, Vila M, Corvol J-C, Vidailhet M, Lehéricy S (2021) The spatiotemporal changes in dopamine,neuromelanin and iron characterizing Parkinson’s disease. Brain 144, 3114–3125. PubMed PMC
Alushaj E, Hemachandra D, Kuurstra A, Menon RS, Ganjavi H, Sharma M, Kashgari A, Barr J, Reisman W, Khan AR, MacDonald PA (2023) Subregional analysis of striatum iron in Parkinson’s disease and rapid eye movement sleep behaviour disorder. Neuroimage Clin 40, 103519. PubMed PMC
Pavese N, Tai YF (2018) Nigrosome imaging and neuromelanin sensitive MRI in diagnostic evaluation of parkinsonism. Mov Disord Clin Pract 5, 131–140. PubMed PMC
Galgani A, Lombardo F, Della Latta D, Martini N, Bonuccelli U, Fornai F, Giorgi FS (2020) Locus coeruleusmagnetic resonance imaging in neurological diseases. Curr Neurol Neurosci Rep 21, 2. PubMed PMC
De Micco R, Agosta F, Basaia S, Siciliano M, Cividini C, Tedeschi G, Filippi M, Tessitore A (2021) Functional connectomics and diseaseprogression in drug-naïve Parkinson’s disease patients. Mov Disord 36, 1603–1616. PubMed
Bejr-Kasem H, Pagonabarraga J, Martínez-Horta S, Sampedro F, Marín-Lahoz J, Horta-Barba A, Aracil-Bolaños I, Pérez-Pérez J, Ángeles Botí M, Campolongo A, Izquierdo C, Pascual-Sedano B, Gómez-Ansón B, Kulisevsky J (2019) Disruption of the default mode network and its intrinsicfunctional connectivity underlies minor hallucinations inParkinson’s disease. Mov Disord 34, 78–86. PubMed
Wolters AF, van de Weijer SCF, Leentjens AFG, Duits AA, Jacobs HIL, Kuijf ML (2019) Resting-state fMRI in Parkinson’s disease patients with cognitive impairment: A meta-analysis. Parkinsonism Relat Disord 62, 16–27. PubMed
Cheng H-C, Ulane CM, Burke RE (2010) Clinical progression in Parkinson disease and the neurobiology of axons. Ann Neurol 67, 715–725. PubMed PMC
Prange S, Theis H, Banwinkler M, van Eimeren T (2022) Molecular imaging in parkinsonian disorders-what’s new and hot? . Brain Sci 12, 1146. PubMed PMC
Brogley JE (2019) DaTQUANT: The future of diagnosing Parkinson disease. J Nucl Med Technol 47, 21–26. PubMed
Pencharz DR, Hanlon P, Chakravartty R, Navalkissoor S, Quigley A-M, Wagner T, Wagner T (2014) Automated quantification with BRASS reduces equivocal reporting of DaTSCAN (123I-FP-CIT) SPECT studies. Nucl Med Rev Cent East Eur 17, 65–69. PubMed
Lanfranchi F, Arnaldi D, Miceli A, Mattioli P, D’Amico F, Raffa S, Donegani MI, Chiola S, Massa F, Pardini M, Di Raimondo T, Sambuceti G, Bauckneht M, Nobili F, Morbelli S (2023) Different z-score cut-offs for striatal binding ratio (SBR) of DaT SPECT are needed to support the diagnosis of Parkinson’s disease (PD) and dementia with Lewy bodies (DLB). Eur J Nucl Med Mol Imaging 50, 1090–1102. PubMed
Af Bjerkén S, Axelsson J, Larsson A, Flygare C, Remes J, Strandberg S, Eriksson L, Bäckström D, Jakobson Mo S (2023) Reliability and validity of visual analysis of [18 F]FE-PE2I PET/CTin early Parkinsonian disease. Nucl Med Commun 44, 397–406. PubMed
Pineda-Pardo JA, Sánchez-Ferro Á, Monje MHG, Pavese N, Obeso JA (2022) Onset pattern of nigrostriatal denervation in earlyParkinson’s disease. Brain 145, 1018–1028. PubMed PMC
Adams JR, van Netten H, Schulzer M, Mak E, Mckenzie J, Strongosky A, Sossi V, Ruth TJ, Lee CS, Farrer M, Gasser T, Uitti RJ, Calne DB, Wszolek ZK, Stoessl AJ (2005) PET in LRRK2 mutations: Comparison to sporadic Parkinson’s disease and evidence for presymptomatic compensation. Brain 128, 2777–2785. PubMed
Sossi V, de la Fuente-Fernández R, Nandhagopal R, Schulzer M, McKenzie J, Ruth TJ, Aasly JO, Farrer MJ, Wszolek ZK, Stoessl JA (2010) Dopamine turnover increases in asymptomatic LRRK2 mutationscarriers. Mov Disord 25, 2717–2723. PubMed
Chahine LM, Brumm MC, Caspell-Garcia C, Oertel W, Mollenhauer B, Amara A, Fernandez-Arcos A, Tolosa E, Simonet C, Hogl B, Videnovic A, Hutten SJ, Tanner C, Weintraub D, Burghardt E, Coffey C, Cho HR, Kieburtz K, Poston KL, Merchant K, Galasko D, Foroud T, Siderowf A, Marek K, Simuni T, Iranzo A (2020) Dopamine transporter imaging predicts clinically-defined α-synucleinopathy in REM sleep behavior disorder. Ann Clin Transl Neurol 8, 201–212. PubMed PMC
Iranzo A, Santamaría J, Valldeoriola F, Serradell M, Salamero M, Gaig C, Niñerola-Baizán A, Sánchez-Valle R, Lladó A, De Marzi R, Stefani A, Seppi K, Pavia J, Högl B, Poewe W, Tolosa E, Lomeña F (2017) Dopamine transporter imaging deficitpredicts early transition to synucleinopathy in idiopathic rapid eyemovement sleep behavior disorder. Ann Neurol 82, 419–428. PubMed
Chahine LM, Iranzo A, Fernández-Arcos A, Simuni T, Seedorff N, Caspell-Garcia C, Amara AW, Comella C, Högl B, Hamilton J, Marek K, Mayer G, Mollenhauer B, Postuma R, Tolosa E, Trenkwalder C, Videnovic A, Oertel W, PPMI Sleep Working Group (2019) Basic clinical features do not predict dopamine transporter binding inidiopathic REM behavior disorder. NPJ Parkinsons Dis 5, 2. PubMed PMC
Kunz D, Stotz S, de Zeeuw J, Papakonstantinou A, Dümchen S, Haberecht M, Plotkin M, Bes F (2023) Prognostic biomarkers in prodromal α-synucleinopathies: DAT binding and REM sleep without atonia. J Neurol Neurosurg Psychiatry 94, 532–540. PubMed PMC
Knudsen K, Fedorova TD, Horsager J, Andersen KB, Skjærbæk C, Berg D, Schaeffer E, Brooks DJ, Pavese N, Van Den Berge N, Borghammer P (2021) Asymmetric dopaminergic dysfunction in brain-first versus body-firstParkinson’s disease subtypes. J Parkinsons Dis 11, 1677–1687. PubMed
Iranzo A, Stefani A, Niñerola-Baizan A, Stokner H, Serradell M, Vilas D, Holzknecht E, Gaig C, Pavia J, Lomeña F, Reyes D, Seppi K, Santamaria J, Högl B, Tolosa E, Poewe W, Sleep InnsbruckBarcelona (SINBAR) Group (2020) Left-hemispheric predominance ofnigrostriatal deficit in isolated REM sleep behavior disorder. Neurology 94, e1605– e1613. PubMed
Siderowf A, Jennings D, Stern M, Seibyl J, Eberly S, Oakes D, Marek K, PARS Investigators (2020) Clinical and imaging progression in the PARS cohort: Long-term follow-up. Mov Disord 35, 1550–1557. PubMed
Marrero-González P, Iranzo A, Bedoya D, Serradell M, Niñerola-Baizán A, Perissinotti A, Gaig C, Vilaseca I, Alobid I, Santamaría J, Mullol J (2020) Prodromal Parkinsondisease in patients with idiopathic hyposmia. J Neurol 267, 3673–3682. PubMed
Löhle M, Wolz M, Beuthien-Baumann B, Oehme L, van den Hoff J, Kotzerke J, Reichmann H, Storch A (2020) Olfactory dysfunction correlates with putaminal dopamine turnover in early de novo Parkinson’s disease. J Neural Transm (Vienna) 127, 9–16. PubMed
Buchert R, Buhmann C, Apostolova I, Meyer T.P, Gallinat J (2019) Nuclear imaging in the diagnosis of clinically uncertain parkinsonian syndromes. Dtsch Arztebl Int 116, 747–754. PubMed PMC
van Eimeren T, Claßen J, Drzezga A, Eggers C, Hilker-Roggendorf R, Klucken J, Koschel J, Meyer PT, Redecker C, Theis H, Buhmann C (2020) [Recommendation for the differentiated use of nuclear medicaldiagnostic for parkinsonian syndromes]. Fortschr NeurolPsychiatr 88, 609–619. PubMed
Beauchamp LC, Dore V, Villemagne VL, Xu S, Finkelstein D, Barnham KJ, Rowe C (2023) Utilizing 18F-AV-133 VMAT2 PET imaging to monitor progressive nigrostriatal degeneration in Parkinson disease. Neurology 101, e2314– e2324. PubMed PMC
Cilia R, Marotta G, Belletti A, Siri C, Pezzoli G (2014) Reversible dopamine transporter reduction in drug-induced Parkinsonism. Mov Disord 29, 575–577. PubMed
Morbelli S, Esposito G, Arbizu J, Barthel H, Boellaard R, Bohnen NI, Brooks DJ, Darcourt J, Dickson JC, Douglas D, Drzezga A, Dubroff J, Ekmekcioglu O, Garibotto V, Herscovitch P, Kuo P, Lammertsma A, Pappata S, Peñuelas I, Seibyl J, Semah F, Tossici-Bolt L, Van deGiessen E, Van Laere K, Varrone A, Wanner M, Zubal G, Law I (2020) EANM practice guideline/SNMMI procedure standard for dopaminergicimaging in Parkinsonian syndromes 1.0. Eur J Nucl Med MolImaging 47, 1885–1912. PubMed PMC
Muzio L, Viotti A, Martino G (2021) Microglia in neuroinflammation and neurodegeneration: From understanding to therapy. Front Neurosci 15, 742065. PubMed PMC
Best L, Ghadery C, Pavese N, Tai YF, Strafella AP (2019) New and old TSPO PET radioligands for imaging brain microglial activation in neurodegenerative disease. Curr Neurol Neurosci Rep 19, 24. PubMed
Gerhard A, Pavese N, Hotton G, Turkheimer F, Es M, Hammers A, Eggert K, Oertel W, Banati RB, Brooks DJ (2006) In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson’s disease. Neurobiol Dis 21, 404–412. PubMed
Stokholm MG, Iranzo A, Østergaard K, Serradell M, Otto M, Svendsen KB, Garrido A, Vilas D, Borghammer P, Santamaria J, Møller A, Gaig C, Brooks DJ, Tolosa E, Pavese N (2017) Assessmentof neuroinflammation in patients with idiopathic rapid-eye-movementsleep behaviour disorder: A case-control study. Lancet Neurol 16, 789–796. PubMed
Stokholm MG, Iranzo A, Østergaard K, Serradell M, Otto M, BacherSvendsen K, Garrido A, Vilas D, Parbo P, Borghammer P, Santamaria J, Møller A, Gaig C, Brooks DJ, Tolosa E, Pavese N (2018) Extrastriatal monoaminergic dysfunction and enhanced microglialactivation in idiopathic rapid eye movement sleep behaviourdisorder. Neurobiol Dis 115, 9–16. PubMed
Gersel Stokholm M, Garrido A, Tolosa E, Serradell M, Iranzo A, Østergaard K, Borghammer P, Møller A, Parbo P, Stær K, Brooks DJ, Martí MJ, Pavese N (2020) Imaging dopamine function and microglia in asymptomaticLRRK2 mutation carriers. J Neurol 267, 2296–2300. PubMed PMC
Mullin S, Stokholm MG, Hughes D, Mehta A, Parbo P, Hinz R, Pavese N, Brooks DJ, Schapira AHV (2021) Brain microglial activation increased in glucocerebrosidase (GBA) mutation carriers without Parkinson’s disease. Mov Disord 36, 774–779. PubMed PMC
Stær K, Iranzo A, Stokholm MG, Østergaard K, Serradell M, Otto M, Svendsen KB, Garrido A, Vilas D, Santamaria J, Møller A, Gaig C, Brooks DJ, Borghammer P, Tolosa E, Pavese N (2020) Cortical cholinergicdysfunction correlates with microglial activation in the substantia innominata in REM sleep behavior disorder. Parkinsonism Relat Disord 81, 89–93. PubMed
Meles SK, Renken RJ, Janzen A, Vadasz D, Pagani M, Arnaldi D, Morbelli S, Nobili F, Mayer G, Leenders KL, Oertel WH, REMPET Study Group (2018) The metabolic pattern of idiopathic REMsleep behavior disorder reflects early-stage Parkinson disease. J NuclMed 59, 1437–1444. PubMed
Orso B, Mattioli P, Yoon E-J, Kim YK, Kim H, Shin JH, Kim R, Liguori C, Famà F, Donniaquio A, Massa F, García DV, Meles SK, Leenders KL, Chiaravalloti A, Pardini M, Bauckneht M, Morbelli S, Nobili F, Lee J-Y, Arnaldi D (2023) Validation of the REM behaviourdisorder phenoconversion-related pattern in an independent cohort. Neurol Sci 44, 3161–3168. PubMed PMC
Mattioli P, Orso B, Liguori C, Famà F, Giorgetti L, DonniaquioA, Massa F, Giberti A, Vállez García D, Meles SK, Leenders KL, Placidi F, Spanetta M, Chiaravalloti A, Camedda R, Schillaci O, Izzi F, Mercuri NB, Pardini M, Bauckneht M, Morbelli S, Nobili F, Arnaldi D (2023) Derivation and validation of aphenoconversion-related pattern in idiopathic rapid eye movementbehavior disorder. Mov Disord 38, 57–67. PubMed PMC
Meles SK, Vadasz D, Renken RJ, Sittig-Wiegand E, Mayer G, Depboylu C, Reetz K, Overeem S, Pijpers A, Reesink FE, van Laar T, Heinen L, Teune LK, Höffken H, Luster M, Kesper K, Adriaanse SM, Booij J, Leenders KL, Oertel WH (2017) FDG PET, dopamine transporter SPECT, and olfaction: Combining biomarkers in REM sleep behavior disorder. Mov Disord 32, 1482–1486. PubMed PMC
Kogan RV, Janzen A, Meles SK, Sittig E, Renken RJ, Gurvits V, Mayer G, Leenders KL, Oertel WH, REMPET Working Group (2021) Four-year follow-up of [18 F]Fluorodeoxyglucose positron emission tomography-based Parkinson’s disease-related pattern expression in 20 patients with isolated rapid eye movement sleep behavior disorder shows prodromal progression. Mov Disord 36, 230–235. PubMed PMC
Carli G, Meles SK, Janzen A, Sittig E, Kogan RV, Perani D, Oertel WH, Leenders KL, REMPET Working Group (2023) Occipital hypometabolism is a risk factor for conversion to Parkinson’s disease in isolated REM sleep behaviour disorder. Eur J Nucl Med Mol Imaging 50, 3290–3301. PubMed PMC
Yoon EJ, Lee J-Y, Kim H, Yoo D, Shin JH, Nam H, Jeon B, Kim YK (2022) Brain metabolism related to mild cognitive impairment and phenoconversion in patients with isolated REM sleep behavior disorder. Neurology 98, e2413– e2424. PubMed PMC
Peng S, Tang C, Schindlbeck K, Rydzinski Y, Dhawan V, Spetsieris PG, Ma Y, Eidelberg D (2021) Dynamic 18F-FPCIT PET: Quantification of Parkinson’s disease metabolic networks and nigrostriatal dopaminergic dysfunction in a single imaging session. J Nucl Med 62, 1775–1782. PubMed PMC
Horsager J, Okkels N, Hansen AK, Damholdt MF, Andersen KH, Fedorova TD, Munk OL, Danielsen EH, Pavese N, Brooks DJ, Borghammer P (2022) Mapping cholinergic synaptic loss in Parkinson’s disease: An [18F]FEOBV PET case-control study. J Parkinsons Dis 12, 2493–2506. PubMed
van der Zee S, Kanel P, Gerritsen MJJ, Boertien JM, Slomp AC, Müller MLTM, Bohnen NI, Spikman JM, van Laar T (2022) Altered cholinergic innervation in de novo Parkinson’s disease with and without cognitive impairment. Mov Disord 37, 713–723. PubMed PMC
Bohnen NI, Roytman S, Kanel P, Müller MLTM, Scott PJH, Frey KA, Albin RL, Koeppe RA (2022) Progression of regional cortical cholinergic denervation in Parkinson’s disease. Brain Commun 4, fcac320. PubMed PMC
Slingerland S, van der Zee S, Carli G, Slomp AC, Boertien JM, d’Angremont E, Bohnen NI, Albin RL, van Laar T (2023) Cholinergic innervation topography in GBA-associated de novo Parkinson’s disease patients, Brain, doi: 10.1093/brain/awad323. PubMed DOI PMC
Staer K, Iranzo A, Terkelsen MH, Stokholm MG, Danielsen EH, Østergaard K, Serradell M, Otto M, Svendsen KB, Garrido A, Vilas D, Santamaria J, Møller A, Gaig C, Brooks DJ, Borghammer P, Tolosa E, Pavese N (2024) Progression of brain cholinergicdysfunction in patients with isolated rapid eye movement sleepbehavior disorder. Eur J Neurol 31, e16101. PubMed PMC
Tan C, Nawaz H, Lageman SK, Cloud LJ, Amara AW, Newman BT, Druzgal TJ, Berman BD, Mukhopadhyay N, Barrett MJ (2023) Cholinergic nucleus 4 degeneration and cognitive impairment in isolated rapid eye movement sleep behavior disorder. Mov Disord 38, 474–479. PubMed PMC
de Natale ER, Wilson H, Politis M (2021) Serotonergic imaging in Parkinson’s disease. Prog Brain Res 261, 303–338. PubMed
Fazio P, Ferreira D, Svenningsson P, Halldin C, Farde L, Westman E, Varrone A (2020) High-resolution PET imaging reveals subtle impairment of the serotonin transporter in an early non-depressed Parkinson’s disease cohort. Eur J Nucl Med Mol Imaging 47, 2407–2416. PubMed PMC
Maillet A, Météreau E, Tremblay L, Favre E, Klinger H, Lhommée E, Le Bars D, Castrioto A, Prange S, Sgambato V, Broussolle E, Krack P, Thobois S (2021) Serotonergic anddopaminergic lesions underlying parkinsonian neuropsychiatric signs. Mov Disord 36, 2888–2900. PubMed
Pavese N, Metta V, Bose SK, Chaudhuri KR, Brooks DJ (2010) Fatigue in Parkinson’s disease is linked to striatal and limbic serotonergic dysfunction. Brain 133, 3434–3443. PubMed
Barber TR, Griffanti L, Muhammed K, Drew DS, Bradley KM, McGowan DR, Crabbe M, Lo C, Mackay CE, Husain M, Hu MT, Klein JC (2018) Apathy in rapid eye movement sleep behaviour disorder is associated with serotonin depletion in the dorsal raphe nucleus. Brain 141, 2848–2854. PubMed PMC
Doppler CEJ, Kinnerup MB, Brune C, Farrher E, Betts M, Fedorova TD, Schaldemose JL, Knudsen K, Ismail R, SegerAD, Hansen AK, Stær K, Fink GR, Brooks DJ, Nahimi A, Borghammer P, Sommerauer M (2021) Regional locuscoeruleus degeneration is uncoupled from noradrenergic terminal loss in Parkinson’s disease. Brain 144, 2732–2744. PubMed
Laurencin C, Lancelot S, Brosse S, Mérida I, Redouté J, Greusard E, Lamberet L, Liotier V, Le Bars D, Costes N, Thobois S, Boulinguez P, Ballanger B (2023) Noradrenergic alterations inParkinson’s disease: A combined 11C-yohimbine PET/neuromelanin MRIstudy, Brain, doi: 10.1093/brain/awad338. PubMed DOI PMC
Knudsen K, Fedorova TD, Hansen AK, Sommerauer M, Otto M, Svendsen KB, Nahimi A, Stokholm MG, Pavese N, Beier CP, Brooks DJ, Borghammer P (2018) In-vivo staging of pathology in REM sleep behaviour disorder: A multimodality imaging case-control study. Lancet Neurol 17, 618–628. PubMed
Brumberg J, Kuzkina A, Lapa C, Mammadova S, Buck A, Volkmann J, Sommer C, Isaias IU, Doppler K (2021) Dermal and cardiac autonomic fiber involvement in Parkinson’s disease and multiple system atrophy. Neurobiol Dis 153, 105332. PubMed
Hawkes CH, Del Tredici K, Braak H (2007) Parkinson’s disease: A dual-hit hypothesis. Neuropathol Appl Neurobiol 33, 599–614. PubMed PMC
Knudsen K, Fedorova TD, Hansen AK, Sommerauer M, Haase A-M, Svendsen KB, Otto M, Østergaard K, Krogh K, Borghammer P (2019) Objectiveintestinal function in patients with idiopathic REM sleep behaviordisorder. Parkinsonism Relat Disord 58, 28–34. PubMed
Siebner TH, Fuglsang S, Madelung CF, Løkkegaard A, Bendtsen F, Hove JD, Damgaard M, Madsen JL, Siebner HR (2022) Gastric emptyingis not delayed and does not correlate with attenuated postprandialblood flow increase in medicated patients with early Parkinson’sdisease. Front Neurol 13, 828069. PubMed PMC
Horsager J, Andersen KB, Knudsen K, Skjærbæk C, Fedorova TD, Okkels N, Schaeffer E, Bonkat SK, Geday J, Otto M, Sommerauer M, Danielsen EH, Bech E, Kraft J, Munk OL, Hansen SD, Pavese N, Göder R, Brooks DJ, Berg D, Borghammer P (2020) Brain-first versus body-first Parkinson’s disease: A multimodal imaging case-controlstudy. Brain 143, 3077–3088. PubMed
Totsune T, Baba T, Sugimura Y, Oizumi H, Tanaka H, Takahashi T, Yoshioka M, Nagamatsu K-I, Takeda A (2023) Nuclear imaging data-driven classification of Parkinson’s disease. Mov Disord 38, 2053–2063. PubMed
Fearon C, Lang AE, Espay AJ (2021) The logic and pitfalls of Parkinson’s disease as “brain-first” versus “body-first” subtypes. Mov Disord 36, 594–598. PubMed
Kim MS, Park DG, An Y-S, Yoon JH (2023) Dual-phase 18 F-FP-CIT positron emission tomography and cardiac 123 I-MIBG scintigraphy of Parkinson’s disease patients with GBA mutations: Evidence of the body-first type? . Eur J Neurol 30, 344–352. PubMed
Park DG, Kang J, An Y-S, Chang J, Yoon JH (2022) Association of plasma α-synuclein with cardiac 123I-MIBG scintigraphy in early Parkinson’s disease. Neurosci Lett 770, 136399. PubMed
Pitton Rissardo J, Fornari Caprara AL (2023) Cardiac 123I-metaiodobenzylguanidine (MIBG) scintigraphy in Parkinson’s disease: A comprehensive review. Brain Sci 13, 1471. PubMed PMC
Bombardieri E, Giammarile F, Aktolun C, Baum RP, Bischof Delaloye A, Maffioli L, Moncayo R, Mortelmans L, Pepe G, Reske SN, Castellani MR, Chiti A, European Association for Nuclear Medicine (2010) 131I/123I-metaiodobenzylguanidine (mIBG) scintigraphy: Procedure guidelines for tumour imaging. Eur J Nucl Med Mol Imaging 37, 2436–2446. PubMed
Stuparu AZ, Jurja S, Stuparu AF, Axelerad A (2023) Narrative review concerning the clinical spectrum of ophthalmological impairments in Parkinson’s disease. Neurol Int 15, 140–161. PubMed PMC
Mailankody P, Lenka A, Pal PK (2019) The role of optical coherence tomography in Parkinsonism: A critical review. J Neurol Sci 403, 67–74. PubMed
Deng Y, Jie C, Wang J, Liu Z, Li Y, Hou X (2022) Evaluation of retina and microvascular changes in the patient with Parkinson’s disease: A systematic review and meta-analysis. Front Med (Lausanne) 9, 957700. PubMed PMC
Rascunà C, Cicero CE, Chisari CG, Russo A, Giuliano L, Castellino N, Terravecchia C, Grillo M, Longo A, Avitabile T, Zappia M, Reibaldi M, Nicoletti A (2021) Retinal thickness andmicrovascular pathway in Idiopathic Rapid eye movement sleepbehaviour disorder and Parkinson’s disease. Parkinsonism RelatDisord 88, 40–45. PubMed
Cerveró A, Sánchez-Rodríguez A, Rivera-Sánchez M, Martínez-Rodríguez I, Sierra M, González-Aramburu I, Gutiérrez-González A, Andrés-Pacheco J, Sánchez-Peláez MV, Casado A, Infante J (2023) Analysis ofretinal nerve layers in idiopathic, LRRK2-associated Parkinson’sdisease and unaffected carriers of G2019S mutation. Parkinsonism Relat Disord 106, 105246. PubMed
Bischof GN, Ewers M, Franzmeier N, Grothe MJ, Hoenig M, Kocagoncu E, Neitzel J, Rowe JB, Strafella A, Drzezga A, van Eimeren T, MINC faculty (2019) Connectomics and molecular imaging in neurodegeneration. Eur J Nucl Med Mol Imaging 46, 2819–2830. PubMed PMC
Chougar L, Arsovic E, Gaurav R, Biondetti E, Faucher A, Valabrègue R, Pyatigorskaya N, Dupont G, Lejeune F-X, Cormier F, Corvol J-C, Vidailhet M, Degos B, Grabli D, Lehéricy S (2022) Regional selectivity of neuromelanin changes in the substantia nigrain atypical parkinsonism. Mov Disord 37, 1245–1255. PubMed
Fan Z, Aman Y, Ahmed I, Chetelat G, Landeau B, Ray Chaudhuri K, Brooks DJ, Edison P (2015) Influence of microglial activation on neuronal function in Alzheimer’s and Parkinson’s disease dementia. Alzheimers Dement 11, 608–621.e7. PubMed
Janzen A, Vadasz D, Booij J, Luster M, Librizzi D, Henrich MT, Timmermann L, Habibi M, Sittig E, Mayer G, Geibl F, Oertel W (2022) Progressive olfactory impairment and cardiac sympathetic denervation in REM sleep behavior disorder. J Parkinsons Dis 12, 1921–1935. PubMed PMC
Smith R, Capotosti F, Schain M, Ohlsson T, Vokali E, Molette J, Touilloux T, Hliva V, Dimitrakopoulos IK, Puschmann A, Jögi J, Svenningsson P, Andréasson M, Sandiego C, Russell DS, Miranda-Azpiazu P, Halldin C, Stomrud E, Hall S, Bratteby K, TampioL’Estrade E, Luthi-Carter R, Pfeifer A, Kosco-Vilbois M, Streffer J, Hansson O (2023) The α-synuclein PET tracer [18F] ACI-12589distinguishes multiple system atrophy from other neurodegenerativediseases. Nat Commun 14, 6750. PubMed PMC
Fernandes Gomes B, Farris CM, Ma Y, Concha-Marambio L, Lebovitz R, Nellgård B, Dalla K, Constantinescu J, Constantinescu R, Gobom J, Andreasson U, Zetterberg H, Blennow K (2023) α-Synucleinseed amplification assay as a diagnostic tool for parkinsoniandisorders. Parkinsonism Relat Disord 117, 105807. PubMed
Early Changes in the Locus Coeruleus in Mild Cognitive Impairment with Lewy Bodies