Degeneration of nigrostriatal dopaminergic neurons in the early to intermediate stage of dementia with Lewy bodies and Parkinson's disease

To investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases. An integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and...

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Published inJournal of the neurological sciences Vol. 449; p. 120660
Main Authors Okitsu, Masato, Sugaya, Keizo, Nakata, Yasuhiro, Kawazoe, Tomoya, Ikezawa, Jun, Okiyama, Ryoichi, Takahashi, Kazushi
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 15.06.2023
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ISSN0022-510X
1878-5883
1878-5883
DOI10.1016/j.jns.2023.120660

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Abstract To investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases. An integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and 123I-FP-CIT dopamine transporter SPECT, and the relationship and laterality of three variables, including neuromelanin-related contrast in the substantia nigra (NRCSN) and locus coeruleus (NRCLC) and the specific binding ratio (SBR) in the striatum, were examined in detail. Patients with DLB and PD and control subjects (n = 29, 52, and 18, respectively) were enrolled. A significantly greater decrease in the SBR in the bilateral hemispheres was observed in DLB than in PD. After adjusting for the interhemispheric asymmetry in neuromelanin-related MRI contrast by using the Z-score, linear regression between the NRCSN and SBR was performed for the most-affected/least-affected sides of the hemispheres as defined by the interhemispheric differences in each variable (SBR, NRCSN, standardized [SBR + NRCSN]). In DLB, the highest, albeit statistically non-significant, correlation was observed in the SBR-based, most-affected side. In PD, the highest correlation was observed in the (SBR + NRCSN)-based, most-affected side, which approximated the value of the clinically-defined, most-affected side. A non-significant correlation was observed only in the (SBR + NRCSN)-based or clinically-defined, least-affected side. Loss of the soma and presynaptic terminals may occur independently in DLB with a large decrease in the presynaptic terminals. The close relationship observed between the degeneration of the soma and presynaptic terminals suggested that axon degeneration may dominate in PD. •An integrative neuroimaging study based on DAT SPECT and 3-Tesla neuromelanin-sensitive MRI was developed.•The correlation of NRCSN with SBR in patients with DLB and PD in the early to intermediate stage of the diseases was found.•Loss of the soma and presynaptic terminals occurred independently in DLB.•A close relationship was found between soma and presynaptic terminal degeneration in PD.
AbstractList AbstractObjectiveTo investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases. MethodsAn integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and 123I-FP-CIT dopamine transporter SPECT, and the relationship and laterality of three variables, including neuromelanin-related contrast in the substantia nigra (NRC SN) and locus coeruleus (NRC LC) and the specific binding ratio (SBR) in the striatum, were examined in detail. Patients with DLB and PD and control subjects ( n = 29, 52, and 18, respectively) were enrolled. ResultsA significantly greater decrease in the SBR in the bilateral hemispheres was observed in DLB than in PD. After adjusting for the interhemispheric asymmetry in neuromelanin-related MRI contrast by using the Z-score, linear regression between the NRC SN and SBR was performed for the most-affected/least-affected sides of the hemispheres as defined by the interhemispheric differences in each variable (SBR, NRC SN, standardized [SBR + NRC SN]). In DLB, the highest, albeit statistically non-significant, correlation was observed in the SBR-based, most-affected side. In PD, the highest correlation was observed in the (SBR + NRC SN)-based, most-affected side, which approximated the value of the clinically-defined, most-affected side. A non-significant correlation was observed only in the (SBR + NRC SN)-based or clinically-defined, least-affected side. ConclusionLoss of the soma and presynaptic terminals may occur independently in DLB with a large decrease in the presynaptic terminals. The close relationship observed between the degeneration of the soma and presynaptic terminals suggested that axon degeneration may dominate in PD.
To investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases. An integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and I-FP-CIT dopamine transporter SPECT, and the relationship and laterality of three variables, including neuromelanin-related contrast in the substantia nigra (NRC ) and locus coeruleus (NRC ) and the specific binding ratio (SBR) in the striatum, were examined in detail. Patients with DLB and PD and control subjects (n = 29, 52, and 18, respectively) were enrolled. A significantly greater decrease in the SBR in the bilateral hemispheres was observed in DLB than in PD. After adjusting for the interhemispheric asymmetry in neuromelanin-related MRI contrast by using the Z-score, linear regression between the NRC and SBR was performed for the most-affected/least-affected sides of the hemispheres as defined by the interhemispheric differences in each variable (SBR, NRC , standardized [SBR + NRC ]). In DLB, the highest, albeit statistically non-significant, correlation was observed in the SBR-based, most-affected side. In PD, the highest correlation was observed in the (SBR + NRC )-based, most-affected side, which approximated the value of the clinically-defined, most-affected side. A non-significant correlation was observed only in the (SBR + NRC )-based or clinically-defined, least-affected side. Loss of the soma and presynaptic terminals may occur independently in DLB with a large decrease in the presynaptic terminals. The close relationship observed between the degeneration of the soma and presynaptic terminals suggested that axon degeneration may dominate in PD.
To investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases.OBJECTIVETo investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases.An integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and 123I-FP-CIT dopamine transporter SPECT, and the relationship and laterality of three variables, including neuromelanin-related contrast in the substantia nigra (NRCSN) and locus coeruleus (NRCLC) and the specific binding ratio (SBR) in the striatum, were examined in detail. Patients with DLB and PD and control subjects (n = 29, 52, and 18, respectively) were enrolled.METHODSAn integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and 123I-FP-CIT dopamine transporter SPECT, and the relationship and laterality of three variables, including neuromelanin-related contrast in the substantia nigra (NRCSN) and locus coeruleus (NRCLC) and the specific binding ratio (SBR) in the striatum, were examined in detail. Patients with DLB and PD and control subjects (n = 29, 52, and 18, respectively) were enrolled.A significantly greater decrease in the SBR in the bilateral hemispheres was observed in DLB than in PD. After adjusting for the interhemispheric asymmetry in neuromelanin-related MRI contrast by using the Z-score, linear regression between the NRCSN and SBR was performed for the most-affected/least-affected sides of the hemispheres as defined by the interhemispheric differences in each variable (SBR, NRCSN, standardized [SBR + NRCSN]). In DLB, the highest, albeit statistically non-significant, correlation was observed in the SBR-based, most-affected side. In PD, the highest correlation was observed in the (SBR + NRCSN)-based, most-affected side, which approximated the value of the clinically-defined, most-affected side. A non-significant correlation was observed only in the (SBR + NRCSN)-based or clinically-defined, least-affected side.RESULTSA significantly greater decrease in the SBR in the bilateral hemispheres was observed in DLB than in PD. After adjusting for the interhemispheric asymmetry in neuromelanin-related MRI contrast by using the Z-score, linear regression between the NRCSN and SBR was performed for the most-affected/least-affected sides of the hemispheres as defined by the interhemispheric differences in each variable (SBR, NRCSN, standardized [SBR + NRCSN]). In DLB, the highest, albeit statistically non-significant, correlation was observed in the SBR-based, most-affected side. In PD, the highest correlation was observed in the (SBR + NRCSN)-based, most-affected side, which approximated the value of the clinically-defined, most-affected side. A non-significant correlation was observed only in the (SBR + NRCSN)-based or clinically-defined, least-affected side.Loss of the soma and presynaptic terminals may occur independently in DLB with a large decrease in the presynaptic terminals. The close relationship observed between the degeneration of the soma and presynaptic terminals suggested that axon degeneration may dominate in PD.CONCLUSIONLoss of the soma and presynaptic terminals may occur independently in DLB with a large decrease in the presynaptic terminals. The close relationship observed between the degeneration of the soma and presynaptic terminals suggested that axon degeneration may dominate in PD.
To investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early to intermediate stage of these diseases. An integrative neuroimaging analysis was developed using 3-Tesla neuromelanin-sensitive MRI and 123I-FP-CIT dopamine transporter SPECT, and the relationship and laterality of three variables, including neuromelanin-related contrast in the substantia nigra (NRCSN) and locus coeruleus (NRCLC) and the specific binding ratio (SBR) in the striatum, were examined in detail. Patients with DLB and PD and control subjects (n = 29, 52, and 18, respectively) were enrolled. A significantly greater decrease in the SBR in the bilateral hemispheres was observed in DLB than in PD. After adjusting for the interhemispheric asymmetry in neuromelanin-related MRI contrast by using the Z-score, linear regression between the NRCSN and SBR was performed for the most-affected/least-affected sides of the hemispheres as defined by the interhemispheric differences in each variable (SBR, NRCSN, standardized [SBR + NRCSN]). In DLB, the highest, albeit statistically non-significant, correlation was observed in the SBR-based, most-affected side. In PD, the highest correlation was observed in the (SBR + NRCSN)-based, most-affected side, which approximated the value of the clinically-defined, most-affected side. A non-significant correlation was observed only in the (SBR + NRCSN)-based or clinically-defined, least-affected side. Loss of the soma and presynaptic terminals may occur independently in DLB with a large decrease in the presynaptic terminals. The close relationship observed between the degeneration of the soma and presynaptic terminals suggested that axon degeneration may dominate in PD. •An integrative neuroimaging study based on DAT SPECT and 3-Tesla neuromelanin-sensitive MRI was developed.•The correlation of NRCSN with SBR in patients with DLB and PD in the early to intermediate stage of the diseases was found.•Loss of the soma and presynaptic terminals occurred independently in DLB.•A close relationship was found between soma and presynaptic terminal degeneration in PD.
ArticleNumber 120660
Author Ikezawa, Jun
Kawazoe, Tomoya
Sugaya, Keizo
Nakata, Yasuhiro
Okiyama, Ryoichi
Takahashi, Kazushi
Okitsu, Masato
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  organization: Department of Neurology, Tokyo Metropolitan Neurological Hospital, Tokyo, Japan
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  surname: Takahashi
  fullname: Takahashi, Kazushi
  organization: Department of Neurology, Tokyo Metropolitan Neurological Hospital, Tokyo, Japan
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CitedBy_id crossref_primary_10_1016_j_prdoa_2024_100242
crossref_primary_10_1016_j_jns_2024_123116
crossref_primary_10_1371_journal_pone_0309885
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Keywords Dopamine transporter scintigraphy
R2
SBR
Parkinson's disease
Neuromelanin-sensitive MRI
MRI
CI
MMSE-J
NRCLC
ROC
NRCSN
SPECT
AUC
ET
Nigrostriatal dopaminergic neuron
PD
DAT
LC
DLB
SN
NRC
Dementia with Lewy bodies
magnetic resonance imaging
NRC LC
locus coeruleus
receiver-operating characteristic
neuromelanin-related contrast in the substantia nigra
NRC SN
substantia nigra
R 2
specific binding ratio
area under the curve
neuromelanin-related contrast in the locus coeruleus
dopamine transporter
Mini Mental State Examination-Japanese
neuromelanin-related contrast
essential tremor
coefficient determination
confidence interval
single-photon emission computed tomography
Language English
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Snippet To investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease (PD) in the early...
AbstractObjectiveTo investigate differences in nigrostriatal dopaminergic neuron degeneration between dementia with Lewy bodies (DLB) and Parkinson's disease...
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SubjectTerms Corpus Striatum - diagnostic imaging
Corpus Striatum - metabolism
Dementia with Lewy bodies
Dopamine transporter scintigraphy
Dopaminergic Neurons - metabolism
Humans
Lewy Body Disease - diagnostic imaging
Lewy Body Disease - metabolism
Neurology
Neuromelanin-sensitive MRI
Nigrostriatal dopaminergic neuron
Parkinson Disease - diagnostic imaging
Parkinson Disease - metabolism
Parkinson's disease
Tomography, Emission-Computed, Single-Photon - methods
Title Degeneration of nigrostriatal dopaminergic neurons in the early to intermediate stage of dementia with Lewy bodies and Parkinson's disease
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https://www.clinicalkey.es/playcontent/1-s2.0-S0022510X2300120X
https://dx.doi.org/10.1016/j.jns.2023.120660
https://www.ncbi.nlm.nih.gov/pubmed/37084522
https://www.proquest.com/docview/2805033475
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