Cited by 20Parkinson's Disease Mechanisms and TreatmentsNeurological disorders and treatmentsDementia and Cognitive Impairment Research

QEEG Signatures are Associated with Nonmotor Dysfunctions in Parkinson's Disease and Atypical Parkinsonism: An Integrative Analysis

Open access
Liu, Hailing, Huang, Zifeng, Deng, Bin, Chang, Zihan, Yang, Xiaohua, Guo, Xingfang, Yuan, Feilan, Yang, Qin +6 more·2023·Aging and disease

Abstract

Parkinson's disease (PD) and atypical parkinsonism (AP), including progressive supranuclear palsy (PSP) and multiple system atrophy (MSA), share similar nonmotor symptoms. Quantitative electroencephalography (QEEG) can be used to examine the nonmotor symptoms. This study aimed to characterize the patterns of QEEG and functional connectivity (FC) that differentiate PD from PSP or MSA, and explore the correlation between the differential QEEG indices and nonmotor dysfunctions in PD and AP. We enrolled 52 patients with PD, 31 with MSA, 22 with PSP, and 50 age-matched health controls to compare QEEG indices among specific brain regions. One-way analysis of variance was applied to assess QEEG indices between groups; Spearman's correlations were used to examine the relationship between QEEG indices and nonmotor symptoms scale (NMSS) and mini-mental state examination (MMSE). FCs using weighted phase lag index were compared between patients with PD and those with MSA/PSP. Patients with PSP revealed higher scores on the NMSS and lower MMSE scores than those with PD and MSA, with similar disease duration. The delta and theta powers revealed a significant increase in PSP, followed by PD and MSA. Patients with PD presented a significantly lower slow-to-fast ratio than those with PSP in the frontal region, while patients with PD presented significantly higher EEG-slowing indices than patients with MSA. The frontal slow-to-fast ratio showed a negative correlation with MMSE scores in patients with PD and PSP, and a positive correlation with NMSS in the perception and mood domain in patients with PSP but not in those with PD. Compared to PD, MSA presented enhanced FC in theta and delta bands in the posterior region, while PSP revealed decreased FC in the delta band within the frontal-temporal cortex. These findings suggest that QEEG might be a useful tool for evaluating the nonmotor dysfunctions in PD and AP. Our QEEG results suggested that with similar disease duration, the cortical neurodegenerative process was likely exacerbated in patients with PSP, followed by those with PD, and lastly in patients with MSA.

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Written from the paper’s full text.

TL;DR

This study compared QEEG spectral power and weighted phase lag index functional connectivity in Parkinson’s disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls, finding distinct slowing and connectivity patterns associated with nonmotor dysfunction. QEEG indices differentiated PD from MSA/PSP and correlated with cognitive, mood, and anxiety measures.

Key findings

  • In 52 PD, 31 MSA, 22 PSP, and 50 age/sex-matched controls, PSP showed higher NMSS and lower MMSE scores than PD and MSA with similar disease duration; delta and theta powers were increased in PSP, followed by PD and MSA (delta P=0.000; theta P=0.004).
  • Global slow-to-fast ratio was higher in PSP than PD or MSA (P=0.000); frontal slow-to-fast ratio was lower in PD than PSP (P=0.003); PD had higher temporal and occipital slow-to-fast ratios and lower parietal/occipital alpha/theta ratios than MSA.
  • Frontal slow-to-fast ratio negatively correlated with MMSE in PD (r=-0.308, p=0.026) and PSP (r=-0.451, P=0.035), and positively correlated with NMSS perception (r=0.465, P=0.029) and mood (r=0.434, P=0.043) domains in PSP; occipital alpha/theta ratio positively correlated with HAMA in MSA (r=0.396, P=0.027).
  • ROC analysis showed occipital alpha/theta ratio AUC 0.799 for PD vs MSA and frontal slow-to-fast ratio AUC 0.717 for PD vs PSP; MSA had enhanced theta/delta functional connectivity in posterior regions, while PSP had decreased theta connectivity in frontal-temporal connections compared with PD.

Methods

  • Retrospective enrollment of patients hospitalized at Zhujiang Hospital of Southern Medical University between 2017 and 2021; final diagnoses made by two neurologists; 52 PD, 31 MSA, 22 PSP, and 50 healthy controls; clinical assessment included MMSE, NMSS, HAMA, HAMD, UPDRS-III, H&Y stage, and LEDD.
  • Resting EEG recorded for 20 min with 19 electrodes; QEEG analysis used FFT absolute spectral power for delta, theta, alpha, and beta bands, slow-to-fast ratio [(delta+theta)/(alpha+beta)], and alpha/theta ratio; functional connectivity used weighted phase lag index.
  • Statistical analysis included ANOVA/Kruskal-Wallis with Bonferroni, Spearman correlations, logistic regression adjusted for confounders, and ROC analysis.

Limitations

  • Stated: sample size was not sufficiently large and precluded certain subgroup analyses; diagnoses were based on clinical probable criteria and not verified by neuropathological examination; no detailed clinical subtypes were specified for PSP.
  • Evident from the text: the study was single-center and retrospective, with cross-sectional correlations that cannot establish causality or longitudinal prediction; the authors also note only a small proportion of PD patients had tremor-dominant manifestations.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.14336/ad.2022.0514

Cites

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Statistics

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Claims the paper makes

0 of 46 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The global slow-to-fast ratio and frontal slow-to-fast ratio differences between PD and PSP were consistent after adjusting for age, LEDD, MMSE, UPDRS-III, NMSS, HAMA, HAMD, and H&Y stage.

    “Logistic regression analyses were conducted to explore the association of the global slow-to-fast ratio (p=0.035) and frontal slow-to-fast ratio (p=0.036) between PD and PSP after adjusting for age, LEDD, MMSE, UPDRS-III, NMSS, HAMA, HMSD, and H&Y stage; the findings revealed that the differences were consistent (Table 2).”
    Quote in the paperSubstantial claim
  • Findingown data

    Patients with PSP presented higher slow-to-fast ratio scores than those with MSA in almost all regions except for the central region.

    “The patients with PSP presented higher scores than those with MSA in almost all regions except for the central region.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Both patients with PD and PSP presented a significant difference in theta and delta ASP compared to those with MSA.

    “Both patients with PD and PSP presented a significant difference in theta and delta ASP compared to those with MSA.”
    Quote in the paperSubstantial claim
  • Findingown data

    In the frontal region, patients with PD presented significantly lower slow-to-fast ratio values than those with PSP.

    “In the frontal region, patients with PD presented significantly lower values than those with PSP (P=0.003).”
    Quote in the paperSubstantial claim
  • Findingown data

    The alpha/theta ratio in parietal and occipital regions between PD and MSA remained associated after adjusting for compounding factors.

    “We explored the association of the alpha/theta ratio in parietal (P=0.029, Table 2) and occipital regions (P=0.001, Table 2) between PD and MSA adjusted for compounding factors and revealed the same results.”
    Quote in the paperSubstantial claim
  • May combine two claims. 28
  • Classified as probably not a substantial claim. 30
  • May combine two claims.

    Findingown data

    Patients with PSP have higher NMSS scores in the attention/memory and perception domains and lower MMSE scores than patients with PD and MSA.

    “Clinical characteristics, such as UPDRS-III and H&Y stage and NMSS scores, in the attention/memory and perception domains, were significantly higher, and MMSE scores were lower in patients with PSP than in those with MSA and PD.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Both delta and theta powers could independently distinguish between PD and MSA after adjusting for age, LEDD, MMSE, UPDRS-III, NMSS, HAMA, HAMD, and H&Y stage.

    “The results showed that both delta (p = 0.001) and theta powers (p = 0.002) could independently distinguish between PD and MSA (Table 2).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Patients with PD revealed significantly higher EEG-slowing and lower EEG-FC than those with MSA.

    “and patients with PD revealed significantly higher EEG-slowing and lower EEG-FC than those with MSA.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The frontal slow-to-fast ratio showed significant positive correlations with cognition in PD and PSP, and with mood/apathy in PSP.

    “We observed that the frontal slow-to-fast ratio showed significant positive correlations with cognition in PD and PSP, and with mood/apathy in PSP.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Alterations in brain FC may precede structural damage and might be a key marker in detecting changes in brain plasticity over short periods in some neurodegenerative diseases.

    “Alterations in the brain FC may precede structural damage and might be a key marker in detecting changes in brain plasticity over short periods in some neurodegenerative diseases [30-32].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [30] Dauwan M, Linszen MMJ, Lemstra AW, Scheltens P, Stam CJ, Sommer IE (2018). EEG-based neurophysiological indicators of hallucinations in Alzheimer's disease: Comparison with dementia with Lewy bodies. Neurobiol Aging, 67:75-83. source

      Not checked in the free run.

    • cites [31] Pelaez Suarez AA, Berrillo Batista S, Pedroso Ibanez I, Casabona Fernandez E, Fuentes Campos M, Chacon LM (2021). EEG-Derived Functional Connectivity Patterns Associated with Mild Cognitive Impairment in Parkinson's Disease. Behav Sci (Basel), 11. source

      Not checked in the free run.

    • cites [32] Attaluri S, Arora M, Madhu LN, Kodali M, Shuai B, Melissari L, et al. (2022). Oral Nano-Curcumin in a Model of Chronic Gulf War Illness Alleviates Brain Dysfunction with Modulation of Oxidative Stress, Mitochondrial Function, Neuroinflammation, Neurogenesis, and Gene Expression. Aging Dis, 13:583-613.

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Patients with PSP showed a higher rate of cognitive, behavioral, and urinary dysfunctions, while those with MSA had higher prevalence of urinary dysfunction, sleep/fatigue symptoms, and mood disorders than patients with PD.

    “Patients with PSP showed a higher rate of cognitive, behavioral, and urinary dysfunctions, while those with MSA had higher prevalence of urinary dysfunction, sleep/fatigue symptoms, and mood disorders than patients with PD [18, 19].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [18] Zhang L, Cao B, Ou R, Wei QQ, Zhao B, Yang J, et al. (2017). Non-motor symptoms and the quality of life in multiple system atrophy with different subtypes. Parkinsonism Relat Disord, 35:63-68. source

      Not checked in the free run.

    • cites [19] Lee CN, Kim M, Lee HM, Jang JW, Lee SM, Kwon DY, et al. (2013). The interrelationship between non-motor symptoms in Atypical Parkinsonism. J Neurol Sci, 327:15-21. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    This study was approved by the Ethics Committee of Zhujiang Hospital of Southern Medical University (NO: 2021-KY-110-02) and complied with ethical standards.

    “This study was approved by the Ethics Committee of Zhujiang Hospital of Southern Medical University (NO: 2021-KY-110-02) and complied with the ethical standards of the 1975 Declaration of Helsinki and the 1999 National Institutes of Health Policy and Guidelines for Human Subjects conduct.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Study design and conductown data

    Logistic regressions were applied to confirm whether QEEG indices could be differential factors between PD and PSP/MSA after adjusting for sex, age, LEDD, MMSE, UPDRS-III, NMSS, HAMA, and HAMD scores.

    “Logistic regressions were applied to confirm whether QEEG indices could be differential factors between PD and PSP/MSA after adjusting for sex, age, LEDD, MMSE, UPDRS-III, NMSS, HAMA, and HAMD scores.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    PSP is characterized by the deposition of four repeat tau inclusions in the caudate, midbrain, thalamus, and frontal cortex.

    “PSP is characterized by the deposition of four repeat tau inclusions in the caudate, midbrain, thalamus, and frontal cortex [33].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [33] Filippi M, Sarasso E, Agosta F (2019). Resting-state Functional MRI in Parkinsonian Syndromes. Mov Disord Clin Pract, 6:104-117. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Cholinergic degeneration may be an important indicator for early cognitive impairment in PD.

    “Neuropathological evidence suggests that cholinergic degeneration may be an important indicator for early cognitive impairment in PD [48-50].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [48] McKinley JW, Shi Z, Kawikova I, Hur M, Bamford IJ, Sudarsana Devi SP, et al. (2019). Dopamine Deficiency Reduces Striatal Cholinergic Interneuron Function in Models of Parkinson's Disease. Neuron, 103:1056-1072 e1056. source

      Not checked in the free run.

    • cites [49] Huntington TE, Srinivasan R (2021). Adeno-Associated Virus Expression of α-Synuclein as a Tool to Model Parkinson's Disease: Current Understanding and Knowledge Gaps. Aging Dis, 12:1120-1137. source

      Not checked in the free run.

    • cites [50] Tian H, Hu Z, Wang C (2022). The Therapeutic Potential of tRNA-derived Small RNAs in Neurodegenerative Disorders. Aging Dis, 13:389-401.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    PSP is associated with a widespread cholinergic deficit resulting from a loss of cholinergic neurons, and with an obvious cholinergic deficiency in the cerebral cortex.

    “Meanwhile, PSP is associated with a widespread cholinergic deficit resulting from a loss of cholinergic neurons, and with an obvious cholinergic deficiency in the cerebral cortex [52].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [52] Javoy-Agid F (1994). Cholinergic and peptidergic systems in PSP. J Neural Transm Suppl, 42:205-218. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The final diagnosis of PD, MSA, and PSP was determined by two neurologists according to updated clinical guidelines.

    “The final diagnosis of PD, MSA, and PSP was determined by two neurologists according to the updated clinical guidelines[37-40].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [37] Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, et al. (1996). Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology, 47:1-9. source

      Not checked in the free run.

    • cites [38] Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, et al. (2008). Second consensus statement on the diagnosis of multiple system atrophy. Neurology, 71:670-676. source

      Not checked in the free run.

    • cites [39] Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. (2015). MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord, 30:1591-1601. source

      Not checked in the free run.

    • cites [40] Hoglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE, et al. (2017). Clinical diagnosis of progressive supranuclear palsy: The movement disorder society criteria. Mov Disord, 32:853-864.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    ASP was logarithmically transformed to achieve homogeneity of variance for normally distributed data.

    “ASP was logarithmically transformed to achieve homogeneity of variance for normally distributed data.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Beta power changes are associated with the severity of motor function, such as dyskinesias and freezing gait, in patients with PD.

    “Studies have revealed that beta power changes are associated with the severity of motor function, such as dyskinesias and freezing gait [28]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [28] Quynh Tran L, Ardi Handojoseno AM, Gilat M, Nghia N, Rifai C, Tran Y, et al. (2016). Detection of gait initiation failure in Parkinson's disease patients using EEG signals. Annu Int Conf IEEE Eng Med Biol Soc, 2016:1599-1602.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The complex interaction between cholinergic and other transmitter systems participates in the pathophysiological mechanism of brain electricity slowing and cognitive decline in neurodegenerative diseases.

    “Studies have shown that the complex interaction between cholinergic and other transmitter systems participates in the pathophysiological mechanism of brain electricity slowing and cognitive decline in neurodegenerative diseases [42-46].”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [42] Kuhl DE, Minoshima S, Fessler JA, Frey KA, Foster NL, Ficaro EP, et al. (1996). In vivo mapping of cholinergic terminals in normal aging, Alzheimer's disease, and Parkinson's disease. Ann Neurol, 40:399-410. source

      Not checked in the free run.

    • cites [43] Bohnen NI, Kaufer DI, Hendrickson R, Ivanco LS, Lopresti BJ, Constantine GM, et al. (2006). Cognitive correlates of cortical cholinergic denervation in Parkinson's disease and parkinsonian dementia. J Neurol, 253:242-247. source

      Not checked in the free run.

    • cites [44] Garcia-Serrano AM, Mohr AA, Philippe J, Skoug C, Spégel P, Duarte JMN (2022). Cognitive Impairment and Metabolite Profile Alterations in the Hippocampus and Cortex of Male and Female Mice Exposed to a Fat and Sugar-Rich Diet are Normalized by Diet Reversal. Aging Dis, 13:267-283. source

      Not checked in the free run.

    • cites [45] Liu N, Tang J, Xue Y, Mok V, Zhang M, Ren X, et al. (2022). EP3 Receptor Deficiency Improves Vascular Remodeling and Cognitive Impairment in Cerebral Small Vessel Disease. Aging Dis, 13:313-328. source

      Not checked in the free run.

    • cites [46] Wang Y, Huang C, Guo Q, Chu H (2022). Aquaporin-4 and Cognitive Disorders. Aging Dis, 13:61-72. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    QEEG could reflect the amount of phosphorylated α-synuclein in the cortex of patients with PD.

    “A study revealed that QEEG could reflect the amount of phosphorylated α-synuclein in the cortex of patients with PD [27].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27] Caviness JN, Lue LF, Hentz JG, Schmitz CT, Adler CH, Shill HA, et al. (2016). Cortical phosphorylated alpha-Synuclein levels correlate with brain wave spectra in Parkinson's disease. Mov Disord, 31:1012-1019. source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    In total, 205 patients with Parkinsonian symptoms were retrospectively reviewed, and after exclusions, 52 patients with PD, 31 with MSA, 22 with PSP, and 50 HC participants were enrolled.

    “In total, 205 patients with Parkinsonian symptoms were retrospectively reviewed. Twenty-nine patients with uncertain diagnoses of probable MSA with cerebellar ataxia (MSA-C), DLB, and CBD were excluded, and 71 patients were ultimately excluded due to excessive artifacts or meeting the exclusion criteria. Consequently, only 52 patients with PD, 31 with MSA, and 22 with PSP and 50 HC participants”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    With similar disease duration, the cortical neurodegenerative process was likely exacerbated in patients with PSP, followed by those with PD, and lastly in patients with MSA.

    “Our QEEG results suggested that with similar disease duration, the cortical neurodegenerative process was likely exacerbated in patients with PSP, followed by those with PD, and lastly in patients with MSA.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The wPLI is a good candidate parameter for revealing synchronized data among connectivity analyses of EEG and magneto-encephalogram signals.

    “In conclusion, among the connectivity analyses of EEG and magneto-encephalogram signals, the wPLI is a good candidate parameter for revealing synchronized data [36].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [36] Vinck M, Oostenveld R, van Wingerden M, Battaglia F, Pennartz CM (2011). An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias. Neuroimage, 55:1548-1565. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    QEEG features provide a valuable variable in distinguishing various etiological dementias, such as DLB, PDD, and AD.

    “Several studies[23-26] have suggested that QEEG features provide a valuable variable in distinguishing various etiological dementias, such as dementia with Lewy bodies (DLB), PD with dementia (PDD), and Alzheimer’s disease (AD).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [23] Stylianou M, Murphy N, Peraza LR, Graziadio S, Cromarty R, Killen A, et al. (2018). Quantitative electroencephalography as a marker of cognitive fluctuations in dementia with Lewy bodies and an aid to differential diagnosis. Clin Neurophysiol, 129:1209-1220. source

      Not checked in the free run.

    • cites [24] van der Zande JJ, Gouw AA, van Steenoven I, van de Beek M, Scheltens P, Stam CJ, et al. (2020). Diagnostic and prognostic value of EEG in prodromal dementia with Lewy bodies. Neurology, 95:e662-e670. source

      Not checked in the free run.

    • cites [25] Botchway BO, Okoye FC, Chen Y, Arthur WE, Fang M (2022). Alzheimer Disease: Recent Updates on Apolipoprotein E and Gut Microbiome Mediation of Oxidative Stress, and Prospective Interventional Agents. Aging Dis, 13:87-102. source

      Not checked in the free run.

    • cites [26] Decourt B, D'Souza GX, Shi J, Ritter A, Suazo J, Sabbagh MN (2022). The Cause of Alzheimer's Disease: The Theory of Multipathology Convergence to Chronic Neuronal Stress. Aging Dis, 13:37-60. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Nonmotor symptoms may vary in PD and AP.

    “Previous studies [16, 17] indicated that nonmotor symptoms may vary in PD and AP.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [16] Hendricks RM, Khasawneh MT (2021). A Systematic Review of Parkinson's Disease Cluster Analysis Research. Aging Dis, 12:1567-1586. source

      Not checked in the free run.

    • cites [17] Leggio L, Paternò G, Vivarelli S, Falzone GG, Giachino C, Marchetti B, et al. (2021). Extracellular Vesicles as Novel Diagnostic and Prognostic Biomarkers for Parkinson's Disease. Aging Dis, 12:1494-1515. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    PSP patients have more severe motor and nonmotor functions than PD patients.

    “First, in the same disease duration, patients with PSP revealed a lower MMSE score and higher UPDRS-III and NMSS scores than those with PD, suggesting severe motor and nonmotor functions in patients with PSP than those with PD.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Study design and conductown data

    The differences in sex, age, and duration were not significant among groups.

    “The differences in sex, age, and duration were not significant.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductown data

    The false discovery rate (FDR) measurement was used to address multiple testing and perform graph theory analysis.

    “The false discovery rate (FDR) measurement provided by the network-based statistic connectome MATLAB package and HERMES toolbox was used to address the problems of multiple testing and perform graph theory analysis.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    In a QEEG study, EEG slowing is frequently reported in patients with PD, and delta and theta global absolute powers were found in patients with PDD.

    “In a QEEG study, EEG slowing is frequently reported in patients with PD, and delta and theta global absolute powers were found in patients with PDD [51].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [51] Fonseca LC, Tedrus GM, Carvas PN, Machado EC (2013). Comparison of quantitative EEG between patients with Alzheimer's disease and those with Parkinson's disease dementia. Clin Neurophysiol, 124:1970-1974. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    An EEG study with transgenic mice demonstrated a close correlation between neuronal accumulation of α-synuclein and slowing of brain oscillations and changes in network excitability.

    “An EEG study with transgenic mice demonstrated a close correlation between neuronal accumulation of α-synuclein and slowing of brain oscillations and changes in network excitability [22, 41].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [22] Colom-Cadena M, Spires-Jones T, Zetterberg H, Blennow K, Caggiano A, DeKosky ST, et al. (2020). The clinical promise of biomarkers of synapse damage or loss in Alzheimer's disease. Alzheimers Res Ther, 12:21. source

      Not checked in the free run.

    • cites [41] Morris M, Sanchez PE, Verret L, Beagle AJ, Guo W, Dubal D, et al. (2015). Network dysfunction in α-synuclein transgenic mice and human Lewy body dementia. Ann Clin Transl Neurol, 2:1012-1028. source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    Pairwise comparisons were conducted by Student's t-test, and FDR-corrected P < 0.05 was considered statistically significant.

    “Pairwise comparisons were conducted by Student’s t-test, and FDR-corrected P < 0.05 was considered statistically significant.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    All participants signed an informed consent form.

    “All participants signed an informed consent form.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    QEEG could demonstrate increased theta power in patients with depression, and increased alpha power or decreased theta/delta power in patients with anxiety.

    “QEEG could demonstrate the increased theta power in patients with depression, and the increased alpha power or decreased theta/delta power in patients with anxiety[54].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [54] Moon SY, Choi YB, Jung HK, Lee YI, Choi SH (2018). Increased Frontal Gamma and Posterior Delta Powers as Potential Neurophysiological Correlates Differentiating Posttraumatic Stress Disorder from Anxiety Disorders. Psychiatry Investig, 15:1087-1093. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The volume of the striatum and brainstem was significantly reduced in MSA.

    “Previous neuroimaging findings showed that the volume of the striatum and brainstem was significantly reduced in MSA [62].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [62] Brenneis C, Seppi K, Schocke MF, Müller J, Luginger E, Bösch S, et al. (2003). Voxel-based morphometry detects cortical atrophy in the Parkinson variant of multiple system atrophy. Mov Disord, 18:1132-1138. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Only a small proportion of patients with PD presented tremor-dominant manifestations.

    “In our study, only a small proportion of patients with PD presented tremor-dominant manifestations.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Study design and conductnone given

    The sample size was not sufficiently large, and the relatively small sample size precluded certain subgroup analyses.

    “First, the sample size was not sufficiently large, and the relatively small sample size precluded certain subgroup analyses.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    The cortical neurodegenerative process was likely exacerbated in patients with PSP, followed by PD and then MSA.

    “Since the disease durations for the three Parkinsonism cases in our study were very similar (Table 1), the QEEG indicators (Figs. 2, 3) and FC network data (Fig. 5) indicated that the cortical neurodegenerative process was likely exacerbated in patients with PSP, followed by PD and then MSA.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    Patients with PSP experience worse cognitive dysfunction and cortical degeneration than PD.

    “further implying that patients with PSP experience worse cognitive dysfunction and cortical degeneration, which was verified by MMSE scores between PD and PSP (Table 1).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    QEEG indices could contribute to a better understanding of the underlying neurophysiology of nonmotor dysfunctions in PD and PSP/MSA.

    “QEEG indices could contribute to a better understanding of the underlying neurophysiology of nonmotor dysfunctions in PD and PSP/MSA.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: QEEG signatures reflect cortical activity and are associated with clinical manifestations, including cognitive impairment, neuropsychiatric disorders, and mental health disorders.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Among all indicators for EEG-slowing, the alpha/theta ratio is more sensitive in the early stage of Parkinsonism.

    “It has been documented that, among all indicators for EEG-slowing, the alpha/theta ratio is more sensitive in the early stage of Parkinsonism [56].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [56] Massa F, Meli R, Grazzini M, Fama F, De Carli F, Filippi L, et al. (2020). Utility of quantitative EEG in early Lewy body disease. Parkinsonism Relat Disord, 75:70-75. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    No detailed clinical subtypes were specified for PSP.

    “Third, no detailed clinical subtypes were specified for PSP.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Compared with healthy people, patients with PD without cognitive impairment showed decreased EEG-FC in the alpha and theta frequencies, while those with PD with mild cognitive impairment showed decreased EEG-FC in alpha in posterior distribution, and delta frequency with a generalized distribution.

    “Compared with healthy people, patients with PD without cognitive impairment showed a decrease EEG-FC in the alpha and theta frequencies, while those with PD with mild cognitive impairment showed decreased EEG-FC in alpha in posterior distribution, and delta frequency with a generalized distribution [60].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [60] Peláez Suárez AA, Berrillo Batista S, Pedroso Ibáñez I, Casabona Fernández E, Fuentes Campos M, Chacón LM (2021). EEG-Derived Functional Connectivity Patterns Associated with Mild Cognitive Impairment in Parkinson's Disease. Behav Sci (Basel), 11. source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Neurodegenerative diseases are usually characterized by a significant reduction in network connectivity, and cortical EEG-FC reflects the intensity of information flow among involved cortical regions.

    “Neurodegenerative diseases are usually characterized by a significant reduction in network connectivity, and cortical EEG-FC reflects the intensity of information flow among involved cortical regions [57-59].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [57] Vecchio F, Miraglia F, Marra C, Quaranta D, Vita MG, Bramanti P, et al. (2014). Human brain networks in cognitive decline: a graph theoretical analysis of cortical connectivity from EEG data. J Alzheimers Dis, 41:113-127. source

      Not checked in the free run.

    • cites [58] Cai M, Dang G, Su X, Zhu L, Shi X, Che S, et al. (2021). Identifying Mild Cognitive Impairment in Parkinson's Disease With Electroencephalogram Functional Connectivity. Front Aging Neurosci, 13:701499. source

      Not checked in the free run.

    • cites [59] Peng W, Zhou R, Sun ZF, Long JW, Gong YQ (2022). Novel Insights into the Roles and Mechanisms of GLP-1 Receptor Agonists against Aging-Related Diseases. Aging Dis, 13:468-490.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The EEG features identified in this study are important indicators for cognition in PD and PSP, mood and apathy in PSP, and anxiety in patients with MSA.

    “Based on our data (Fig. 4), we propose that the EEG features identified in this study are important indicators for cognition in PD and PSP, mood and apathy in PSP, and anxiety in patients with MSA.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: QEEG signatures reflect cortical activity and are associated with clinical manifestations, including cognitive impairment, neuropsychiatric disorders, and mental health disorders.
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    An in-depth understanding of QEEG-FC may contribute to understanding the different neuro-pathogenesis of PD and AP.

    “An in-depth understanding of QEEG-FC may contribute to understanding the different neuro-pathogenesis of PD and AP.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    Cortical synaptic function is likely deteriorated in patients with PSP, followed by PD and then MSA.

    “These results also suggest that cortical synaptic function is likely deteriorated in patients with PSP, followed by PD and then MSA.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    MSA presents with less cortical degeneration and might explain the preservation of cognitive function in most MSA cases.

    “In our study, these findings (Fig. 3, 5A, 5B) strongly suggest that MSA presents with less cortical degeneration and might explain the preservation of cognitive function in most MSA cases.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    The changes and differences in EEG-FC between the PD and PSP/MSA groups can be interpreted due to pathophysiological changes, and QEEG indices provide a novel tool to distinguish the underlying neuropathogenesis between PD and PSP/MSA.

    “The changes and differences in EEG-FC between the PD and PSP/MSA groups can be interpreted due to pathophysiological changes, and QEEG indices provide a novel tool to distinguish the underlying neuropathogenesis between PD and PSP/MSA.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    The diagnosis of PD, PSP, and MSA was based on clinical probable diagnosis criteria and was not verified by neuropathological examination.

    “Second, the diagnosis of PD, PSP, and MSA was based on the clinical probable diagnosis criteria and was not verified by neuropathological examination.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    EEG-FC is related to the pathophysiological mechanisms and progression of PD.

    “It is suggested that EEG-FC is related to the pathophysiological mechanisms and progression of PD.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    Pairwise comparisons were conducted by Student's t-test, and false discovery rate (FDR)-corrected P < 0.05 was considered significant.

    “Pairwise comparisons are conducted by Student’s t-test, and false discovery rate (FDR)-corrected P < 0.05 is considered significant.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationown data

    These findings shed light on the possible mechanisms underlying the relationships between QEEG indicator activity and nonmotor dysfunctions in PD and AP, notably the involvement of different processes in cortical degeneration.

    “These findings shed light on the possible mechanisms underlying the relationships between QEEG indicator activity and nonmotor dysfunctions in PD and AP, notably the involvement of different processes in cortical degeneration.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: QEEG signatures reflect cortical activity and are associated with clinical manifestations, including cognitive impairment, neuropsychiatric disorders, and mental health disorders.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Patients with AD with hallucination showed greater delta power compared with those without hallucination.

    “Moreover, patients with AD with hallucination showed greater delta power compared with those without hallucination [55]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [55] Edwards-Lee T, Cook I, Fairbanks L, Leuchter A, Cummings JL (2000). Quantitative electroencephalographic correlates of psychosis in Alzheimer disease. Neuropsychiatry Neuropsychol Behav Neurol, 13:163-170.

      Not checked in the free run.

49 of 49
  • The paper relies on this without support.

    QEEG has not been performed to identify differences in nonmotor dysfunctions among various types of Parkinsonisms.

    “However, QEEG have not been performed to identify differences in nonmotor dysfunctions among various types of Parkinsonisms.”
  • The paper relies on this without support.

    There is no literature using EEG-FC to explore the differences between PD and AP.

    “However, there is no literature using EEG-FC to explore the differences between PD and AP.”
  • The paper relies on this without support.

    PD and AP share similar nonmotor symptoms.

    “Parkinson’s disease (PD) and atypical parkinsonism (AP), including progressive supranuclear palsy (PSP) and multiple system atrophy (MSA), share similar nonmotor symptoms.”
  • The paper relies on this without support.

    EEG-FC between PD and atypical parkinsonism was not available in previous studies.

    “EEG-FC between PD and atypical parkinsonism was not available in previous studies.”
  • The paper relies on this without support.

    QEEG signatures reflect cortical activity and are associated with clinical manifestations, including cognitive impairment, neuropsychiatric disorders, and mental health disorders.

    “QEEG signatures reflected the cortical activity and were associated with clinical manifestations, including cognitive impairment, neuropsychiatric disorders, and mental health disorders.”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Conclusion reverses the reported correlation with MMSE

    Major

    The conclusion calls the frontal slow-to-fast ratio's correlation with cognition positive in PD and PSP, whereas the reported MMSE correlations are negative in both groups.

  • PSP connectivity decrease is assigned to different frequency bands

    Major

    The abstract places the decreased PSP connectivity in the delta band, while the Figure 5 caption identifies it as theta-band connectivity.

  • Theta power is described as highest in PSP, but Table 1 shows a higher PD mean

    Major

    The text ranks PSP above PD for theta power, while Table 1 reports 1.65 for PSP and 1.66 for PD.

  • Delta post-hoc direction conflicts with the group means

    Minor

    Table 1 labels MSA as greater than PSP (B>C), but its reported delta means are 1.66 for MSA and 1.68 for PSP.

  • Occipital slow-to-fast ROC P value differs between text and table

    Minor

    For the PD-MSA occipital slow-to-fast ROC result, the text gives p=0.002, whereas Table 3 gives 0.005.

  • Narrative and table give different age summaries

    Minor

    The narrative and Table 1 disagree on the PD mean and standard deviation, and on the PSP and control standard deviations.

  • Theta post-hoc direction conflicts with the group means

    Minor

    Table 1 labels MSA as greater than PSP (B>C), but its reported theta means are 1.63 for MSA and 1.65 for PSP.

  • Discussion describes a decreased frontal slow-to-fast ratio in PSP

    Minor

    In the discussion of distinguishing PSP from PD, the ratio is described as decreased, but Table 1 reports a higher frontal ratio in PSP (1.22) than in PD (1.17).

8 of 8

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Peláez Suárez AA, Berrillo Batista S, Pedroso Ibáñez I, Casabona Fernández E, Fuentes Campos M, Chacón LM (2021). EEG-Derived Functional Connectivity Patterns Associated with Mild Cognitive Impairment in Parkinson's Disease. Behav Sci (Basel), 11. · DOI · Paper page

Cited by

Sorted by citations

Authors
Liu, H., Huang, Z., Deng, B., Chang, Z., Yang, X., Guo, X., Yuan, F., Yang, Q., Wang, L., Zou, H., Li, M., Zhu, Z., Jin, K., & Wang, Q.
Affiliations
  • Zhujiang Hospital (CN)
  • Guangdong General Hospital (CN)
  • Guangzhou First People's Hospital (CN)
  • University of North Texas Health Science Center (US)
Corresponding author
Wang, Qing
Venue
Aging and disease
Published
2023
Volume
14
Issue
1
Pages
204
ISSN
2152-5250 (ISSN-L)
OpenAlex
W4313038320
Cited by
20
References
68
Citations by year
2026: 7 · 2025: 4 · 2024: 4 · 2023: 5
FWCI
1.71
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Aging and Disease (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China (81873777, 82071414)
  • Natural Science Foundation of Guangdong Province (2017A030311010)
  • Science and Technology Planning Project of Guangdong Province
Topics
  • Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
  • Health Sciences › Medicine › Neurology › Neurological disorders and treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Keywords
Parkinson's disease, atypical parkinsonism, progressive supranuclear palsy, multiple system atrophy, non-motor symptoms, quantitative EEG, functional connectivity, weighted phase lag index, delta power, theta power, frontal lobe, cognitive impairment, mood, cortical neurodegeneration

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