Skip to main content
Erschienen in: Journal of Neurology 12/2022

06.08.2022 | Original Communication

Associated factors and abnormal dorsal raphe nucleus connectivity patterns of freezing of gait in Parkinson’s disease

verfasst von: Lingling Lv, Hainan Zhang, Xuling Tan, Zhe Long, Lixia Qin, Rongrong Bai, Qile Xiao, Ziwei Wu, Shenglan Hu, Changlian Tan, Haiyan Liao, Weiqian Yan, Beisha Tang, Feng Ren, Chunyu Wang

Erschienen in: Journal of Neurology | Ausgabe 12/2022

Einloggen, um Zugang zu erhalten

Abstract

Background

Freezing of gait (FOG) is a common, disabling symptom of Parkinson’s disease (PD), and its exact pathophysiological mechanism is still poorly understood. The control of gait is a complex process that may be influenced by emotions modulated by serotonergic networks. Therefore, this study aimed to determine factors associated with FOG in PD patients and to evaluate the importance of the dorsal raphe nucleus (DRN; central node in the serotoninergic system) in FOG pathophysiology.

Methods

We combined cross-sectional survey data from 453 PD patients. According to the Freezing of Gait Questionnaire (FOGQ), patients were divided into two groups: the “PD with frozen gait (PD-FOG)” and “PD without frozen gait (PD-nFOG)” groups. Demographic characteristics, clinical features, and motor and nonmotor symptoms (NMS) assessments of PD patients were recorded. Univariate statistical analysis was performed between the two groups, and then regression analysis was performed on related factors. We also acquired resting-state functional MRI (rs-fMRI) data from 20 PD-FOG, 21 PD-nFOG, and 22 healthy controls (HCs) who were randomly chosen. We defined seeds in the DRN to evaluate functional connectivity (FC) patterns.

Results

The overall frequency of FOG was 11.9% patients in the PD-FOG group were older, had a longer disease duration, had a higher levodopa equivalent daily dose, had more severe motor symptoms and worse quality of life, had a higher proportion of dyskinesia, wearing-off and postural instability/gait difficulty (PIGD) clinical phenotype, and experienced more depression and impaired sleep function than those in the PD-nFOG group. Logistic regression analysis showed that H&Ystage ≥ 3, UPDRS-III scores, PIGD clinical phenotype and excessive daytime sleepiness were associated with FOG. In addition, there was significantly lower FC between the DRN and some cortical structures, including the supplementary motor area (SMA), left superior frontal gyrus (SFG), and left median cingulated cortex (MCC) in PD-FOG patients than HCs and PD-nFOG patients.

Conclusions

These results demonstrate that the severity of PD and PIGD clinical phenotype are associated factors for freezing and that DRN dysfunction may play a key role in PD-related NMS and FOG. An abnormal cortical and brainstem networks may contribute to the mechanisms underlying FOG.
Literatur
1.
Zurück zum Zitat Cucca A, Biagioni MC, Fleisher JE, Agarwal S, Son A, Kumar P et al (2016) Freezing of gait in Parkinson’s disease: from pathophysiology to emerging therapies. Neurodegener Dis Manag 6(5):431–446PubMedCrossRef Cucca A, Biagioni MC, Fleisher JE, Agarwal S, Son A, Kumar P et al (2016) Freezing of gait in Parkinson’s disease: from pathophysiology to emerging therapies. Neurodegener Dis Manag 6(5):431–446PubMedCrossRef
2.
Zurück zum Zitat Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR (2015) Freezing of gait: a practical approach to management. Lancet Neurol 14(7):768–778PubMedCrossRef Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR (2015) Freezing of gait: a practical approach to management. Lancet Neurol 14(7):768–778PubMedCrossRef
3.
Zurück zum Zitat Rahman S, Griffin HJ, Quinn NP, Jahanshahi M (2008) The factors that induce or overcome freezing of gait in Parkinson’s disease. Behav Neurol 19(3):127–136PubMedPubMedCentralCrossRef Rahman S, Griffin HJ, Quinn NP, Jahanshahi M (2008) The factors that induce or overcome freezing of gait in Parkinson’s disease. Behav Neurol 19(3):127–136PubMedPubMedCentralCrossRef
4.
Zurück zum Zitat Delval A, Snijders AH, Weerdesteyn V, Duysens JE, Defebvre L, Giladi N et al (2010) Objective detection of subtle freezing of gait episodes in Parkinson’s disease. Mov Disord 25(11):1684–1693PubMedCrossRef Delval A, Snijders AH, Weerdesteyn V, Duysens JE, Defebvre L, Giladi N et al (2010) Objective detection of subtle freezing of gait episodes in Parkinson’s disease. Mov Disord 25(11):1684–1693PubMedCrossRef
5.
Zurück zum Zitat Morris ME, Iansek R, Galna B (2008) Gait festination and freezing in Parkinson’s disease: pathogenesis and rehabilitation. Mov Disord 23(Suppl 2):S451–S460PubMedCrossRef Morris ME, Iansek R, Galna B (2008) Gait festination and freezing in Parkinson’s disease: pathogenesis and rehabilitation. Mov Disord 23(Suppl 2):S451–S460PubMedCrossRef
6.
Zurück zum Zitat Delgado-Alvarado M, Marano M, Santurtun A, Urtiaga-Gallano A, Tordesillas-Gutierrez D, Infante J (2020) Nonpharmacological, nonsurgical treatments for freezing of gait in Parkinson’s disease: a systematic review. Mov Disord 35(2):204–214PubMedCrossRef Delgado-Alvarado M, Marano M, Santurtun A, Urtiaga-Gallano A, Tordesillas-Gutierrez D, Infante J (2020) Nonpharmacological, nonsurgical treatments for freezing of gait in Parkinson’s disease: a systematic review. Mov Disord 35(2):204–214PubMedCrossRef
7.
Zurück zum Zitat Ebersbach G, Moreau C, Gandor F, Defebvre L, Devos D (2013) Clinical syndromes: Parkinsonian gait. Mov Disord 28(11):1552–1559PubMedCrossRef Ebersbach G, Moreau C, Gandor F, Defebvre L, Devos D (2013) Clinical syndromes: Parkinsonian gait. Mov Disord 28(11):1552–1559PubMedCrossRef
8.
Zurück zum Zitat Smulders K, Esselink RA, Bloem BR, Cools R (2015) Freezing of gait in Parkinson’s disease is related to impaired motor switching during stepping. Mov Disord 30(8):1090–1097PubMedCrossRef Smulders K, Esselink RA, Bloem BR, Cools R (2015) Freezing of gait in Parkinson’s disease is related to impaired motor switching during stepping. Mov Disord 30(8):1090–1097PubMedCrossRef
9.
Zurück zum Zitat Ou R, Guo X, Song W, Cao B, Yang J, Wei Q et al (2014) Freezing of gait in Chinese patients with Parkinson disease. J Neurol Sci 345(1–2):56–60PubMedCrossRef Ou R, Guo X, Song W, Cao B, Yang J, Wei Q et al (2014) Freezing of gait in Chinese patients with Parkinson disease. J Neurol Sci 345(1–2):56–60PubMedCrossRef
10.
Zurück zum Zitat Contreras A, Grandas F (2012) Risk factors for freezing of gait in Parkinson’s disease. J Neurol Sci 320(1–2):66–71PubMedCrossRef Contreras A, Grandas F (2012) Risk factors for freezing of gait in Parkinson’s disease. J Neurol Sci 320(1–2):66–71PubMedCrossRef
11.
Zurück zum Zitat Banks SJ, Bayram E, Shan G, LaBelle DR, Bluett B (2019) Non-motor predictors of freezing of gait in Parkinson’s disease. Gait Posture 68:311–316PubMedCrossRef Banks SJ, Bayram E, Shan G, LaBelle DR, Bluett B (2019) Non-motor predictors of freezing of gait in Parkinson’s disease. Gait Posture 68:311–316PubMedCrossRef
12.
Zurück zum Zitat Dujardin K, Sgambato V (2020) Neuropsychiatric disorders in Parkinson’s disease: What do we know about the role of dopaminergic and non-dopaminergic systems? Front Neurosci 14:25PubMedPubMedCentralCrossRef Dujardin K, Sgambato V (2020) Neuropsychiatric disorders in Parkinson’s disease: What do we know about the role of dopaminergic and non-dopaminergic systems? Front Neurosci 14:25PubMedPubMedCentralCrossRef
14.
Zurück zum Zitat Miguelez C, Morera-Herreras T, Torrecilla M, Ruiz-Ortega JA, Ugedo L (2014) Interaction between the 5-HT system and the basal ganglia: functional implication and therapeutic perspective in Parkinson’s disease. Front Neural Circuits 8:21PubMedPubMedCentralCrossRef Miguelez C, Morera-Herreras T, Torrecilla M, Ruiz-Ortega JA, Ugedo L (2014) Interaction between the 5-HT system and the basal ganglia: functional implication and therapeutic perspective in Parkinson’s disease. Front Neural Circuits 8:21PubMedPubMedCentralCrossRef
15.
Zurück zum Zitat Briand LA, Gritton H, Howe WM, Young DA, Sarter M (2007) Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog Neurobiol 83(2):69–91PubMedPubMedCentralCrossRef Briand LA, Gritton H, Howe WM, Young DA, Sarter M (2007) Modulators in concert for cognition: modulator interactions in the prefrontal cortex. Prog Neurobiol 83(2):69–91PubMedPubMedCentralCrossRef
16.
Zurück zum Zitat Mirelman A, Bonato P, Camicioli R, Ellis TD, Giladi N, Hamilton JL et al (2019) Gait impairments in Parkinson’s disease. Lancet Neurol 18(7):697–708PubMedCrossRef Mirelman A, Bonato P, Camicioli R, Ellis TD, Giladi N, Hamilton JL et al (2019) Gait impairments in Parkinson’s disease. Lancet Neurol 18(7):697–708PubMedCrossRef
17.
Zurück zum Zitat Maillet A, Pollak P, Debu B (2012) Imaging gait disorders in parkinsonism: a review. J Neurol Neurosurg Psychiatry 83(10):986–993PubMedCrossRef Maillet A, Pollak P, Debu B (2012) Imaging gait disorders in parkinsonism: a review. J Neurol Neurosurg Psychiatry 83(10):986–993PubMedCrossRef
18.
Zurück zum Zitat Pozzi NG, Canessa A, Palmisano C, Brumberg J, Steigerwald F, Reich MM et al (2019) Freezing of gait in Parkinson’s disease reflects a sudden derangement of locomotor network dynamics. Brain 142(7):2037–2050PubMedPubMedCentralCrossRef Pozzi NG, Canessa A, Palmisano C, Brumberg J, Steigerwald F, Reich MM et al (2019) Freezing of gait in Parkinson’s disease reflects a sudden derangement of locomotor network dynamics. Brain 142(7):2037–2050PubMedPubMedCentralCrossRef
19.
Zurück zum Zitat Okuma Y, Yanagisawa N (2008) The clinical spectrum of freezing of gait in Parkinson’s disease. Mov Disord 23(Suppl 2):S426–S430PubMedCrossRef Okuma Y, Yanagisawa N (2008) The clinical spectrum of freezing of gait in Parkinson’s disease. Mov Disord 23(Suppl 2):S426–S430PubMedCrossRef
20.
Zurück zum Zitat Lewis SJ, Shine JM (2016) The next step: a common neural mechanism for freezing of gait. Neuroscientist 22(1):72–82PubMedCrossRef Lewis SJ, Shine JM (2016) The next step: a common neural mechanism for freezing of gait. Neuroscientist 22(1):72–82PubMedCrossRef
21.
Zurück zum Zitat Youn J, Lee JM, Kwon H, Kim JS, Son TO, Cho JW (2015) Alterations of mean diffusivity of pedunculopontine nucleus pathway in Parkinson’s disease patients with freezing of gait. Parkinsonism Relat Disord 21(1):12–17PubMedCrossRef Youn J, Lee JM, Kwon H, Kim JS, Son TO, Cho JW (2015) Alterations of mean diffusivity of pedunculopontine nucleus pathway in Parkinson’s disease patients with freezing of gait. Parkinsonism Relat Disord 21(1):12–17PubMedCrossRef
23.
Zurück zum Zitat Snijders AH, Leunissen I, Bakker M, Overeem S, Helmich RC, Bloem BR et al (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134(Pt 1):59–72PubMedCrossRef Snijders AH, Leunissen I, Bakker M, Overeem S, Helmich RC, Bloem BR et al (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134(Pt 1):59–72PubMedCrossRef
24.
Zurück zum Zitat Schweder PM, Hansen PC, Green AL, Quaghebeur G, Stein J, Aziz TZ (2010) Connectivity of the pedunculopontine nucleus in parkinsonian freezing of gait. NeuroReport 21(14):914–916PubMedCrossRef Schweder PM, Hansen PC, Green AL, Quaghebeur G, Stein J, Aziz TZ (2010) Connectivity of the pedunculopontine nucleus in parkinsonian freezing of gait. NeuroReport 21(14):914–916PubMedCrossRef
25.
Zurück zum Zitat 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(12):1591–1601PubMedCrossRef 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(12):1591–1601PubMedCrossRef
26.
Zurück zum Zitat Giladi N, Tal J, Azulay T, Rascol O, Brooks DJ, Melamed E et al (2009) Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord 24(5):655–661PubMedCrossRef Giladi N, Tal J, Azulay T, Rascol O, Brooks DJ, Melamed E et al (2009) Validation of the freezing of gait questionnaire in patients with Parkinson’s disease. Mov Disord 24(5):655–661PubMedCrossRef
27.
Zurück zum Zitat Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653PubMedCrossRef Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653PubMedCrossRef
28.
Zurück zum Zitat Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P et al (2008) Movement Disorder Society-sponsored revision of the unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23(15):2129–2170PubMedCrossRef Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P et al (2008) Movement Disorder Society-sponsored revision of the unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23(15):2129–2170PubMedCrossRef
29.
Zurück zum Zitat Hoehn M, Yahr MD (1967) Parkinsonism: onset, progression, and mortality. Neurology 17(5):427–442PubMedCrossRef Hoehn M, Yahr MD (1967) Parkinsonism: onset, progression, and mortality. Neurology 17(5):427–442PubMedCrossRef
30.
Zurück zum Zitat Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P et al (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22(13):1901–1911PubMedCrossRef Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P et al (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22(13):1901–1911PubMedCrossRef
31.
Zurück zum Zitat Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198PubMedCrossRef Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198PubMedCrossRef
32.
Zurück zum Zitat Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389PubMedCrossRef Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389PubMedCrossRef
33.
Zurück zum Zitat Millar Vernetti P, Perez Lloret S, Rossi M, Cerquetti D, Merello M (2012) Validation of a new scale to assess olfactory dysfunction in patients with Parkinson’s disease. Parkinsonism Relat Disord 18(4):358–361PubMedCrossRef Millar Vernetti P, Perez Lloret S, Rossi M, Cerquetti D, Merello M (2012) Validation of a new scale to assess olfactory dysfunction in patients with Parkinson’s disease. Parkinsonism Relat Disord 18(4):358–361PubMedCrossRef
34.
Zurück zum Zitat Chaudhuri KR, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Mathew R et al (2002) The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73(6):629–635PubMedPubMedCentralCrossRef Chaudhuri KR, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Mathew R et al (2002) The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73(6):629–635PubMedPubMedCentralCrossRef
35.
Zurück zum Zitat Shen SS, Shen Y, Xiong KP, Chen J, Mao CJ, Huang JY et al (2014) Validation study of REM sleep behavior disorder questionnaire-Hong Kong (RBDQ-HK) in east China. Sleep Med 15(8):952–958PubMedCrossRef Shen SS, Shen Y, Xiong KP, Chen J, Mao CJ, Huang JY et al (2014) Validation study of REM sleep behavior disorder questionnaire-Hong Kong (RBDQ-HK) in east China. Sleep Med 15(8):952–958PubMedCrossRef
36.
Zurück zum Zitat Simuni T, Caspell-Garcia C, Coffey C, Chahine LM, Lasch S, Oertel WH et al (2015) Correlates of excessive daytime sleepiness in de novo Parkinson’s disease: a case control study. Mov Disord 30(10):1371–1381PubMedPubMedCentralCrossRef Simuni T, Caspell-Garcia C, Coffey C, Chahine LM, Lasch S, Oertel WH et al (2015) Correlates of excessive daytime sleepiness in de novo Parkinson’s disease: a case control study. Mov Disord 30(10):1371–1381PubMedPubMedCentralCrossRef
37.
Zurück zum Zitat Peto V, Jenkinson C, Fitzpatrick R, Greenhall R (1995) The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Mov Disord 3:241–248 Peto V, Jenkinson C, Fitzpatrick R, Greenhall R (1995) The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Mov Disord 3:241–248
38.
Zurück zum Zitat Xin HW, Fang XC, Zhu LM, Xu T, Fei GJ, Wang ZF et al (2014) Diagnosis of functional constipation: agreement between Rome III and Rome II criteria and evaluation for the practicality. J Dig Dis 15(6):314–320PubMedPubMedCentralCrossRef Xin HW, Fang XC, Zhu LM, Xu T, Fei GJ, Wang ZF et al (2014) Diagnosis of functional constipation: agreement between Rome III and Rome II criteria and evaluation for the practicality. J Dig Dis 15(6):314–320PubMedPubMedCentralCrossRef
39.
Zurück zum Zitat Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord 28(5):668–670PubMedCrossRef Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord 28(5):668–670PubMedCrossRef
40.
Zurück zum Zitat Yan C, Wang X, Zuo X, Zang Y (2016) DPABI: Data processing and analysis for (resting-state) brain imaging. Neuroinformatics 14(3):339–351PubMedCrossRef Yan C, Wang X, Zuo X, Zang Y (2016) DPABI: Data processing and analysis for (resting-state) brain imaging. Neuroinformatics 14(3):339–351PubMedCrossRef
41.
Zurück zum Zitat Yan CG, Cheung B, Kelly C, Colcombe S, Craddock RC, Di Martino A et al (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76:183–201PubMedCrossRef Yan CG, Cheung B, Kelly C, Colcombe S, Craddock RC, Di Martino A et al (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76:183–201PubMedCrossRef
42.
Zurück zum Zitat Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13PubMedPubMedCentral Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13PubMedPubMedCentral
44.
Zurück zum Zitat Amboni M, Stocchi F, Abbruzzese G, Morgante L, Onofrj M, Ruggieri S et al (2015) Prevalence and associated features of self-reported freezing of gait in Parkinson disease: the DEEP FOG study. Parkinsonism Relat Disord 21(6):644–649PubMedCrossRef Amboni M, Stocchi F, Abbruzzese G, Morgante L, Onofrj M, Ruggieri S et al (2015) Prevalence and associated features of self-reported freezing of gait in Parkinson disease: the DEEP FOG study. Parkinsonism Relat Disord 21(6):644–649PubMedCrossRef
45.
Zurück zum Zitat Macht M, Kaussner Y, Moller JC, Stiasny-Kolster K, Eggert KM, Kruger HP et al (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22(7):953–956PubMedCrossRef Macht M, Kaussner Y, Moller JC, Stiasny-Kolster K, Eggert KM, Kruger HP et al (2007) Predictors of freezing in Parkinson’s disease: a survey of 6,620 patients. Mov Disord 22(7):953–956PubMedCrossRef
46.
Zurück zum Zitat Takahashi M, Tabu H, Ozaki A, Hamano T, Takeshima T, group Rs (2019) Antidepressants for depression, apathy, and gait instability in Parkinson’s disease: a multicenter randomized study. Intern Med 58(3):361–368PubMedCrossRef Takahashi M, Tabu H, Ozaki A, Hamano T, Takeshima T, group Rs (2019) Antidepressants for depression, apathy, and gait instability in Parkinson’s disease: a multicenter randomized study. Intern Med 58(3):361–368PubMedCrossRef
47.
Zurück zum Zitat Devos D, Defebvre L, Bordet R (2010) Dopaminergic and non-dopaminergic pharmacological hypotheses for gait disorders in Parkinson’s disease. Fundam Clin Pharmacol 24(4):407–421PubMedCrossRef Devos D, Defebvre L, Bordet R (2010) Dopaminergic and non-dopaminergic pharmacological hypotheses for gait disorders in Parkinson’s disease. Fundam Clin Pharmacol 24(4):407–421PubMedCrossRef
48.
Zurück zum Zitat Paulus W, Jellinger K (1991) The neuropathologic basis of different clinical subgroups of Parkinson’s disease. J Neuropathol Exp Neurol 50(6):743–755PubMedCrossRef Paulus W, Jellinger K (1991) The neuropathologic basis of different clinical subgroups of Parkinson’s disease. J Neuropathol Exp Neurol 50(6):743–755PubMedCrossRef
49.
Zurück zum Zitat Herman T, Shema-Shiratzky S, Arie L, Giladi N, Hausdorff JM (2019) Depressive symptoms may increase the risk of the future development of freezing of gait in patients with Parkinson’s disease: findings from a 5-year prospective study. Parkinsonism Relat Disord 60:98–104PubMedCrossRef Herman T, Shema-Shiratzky S, Arie L, Giladi N, Hausdorff JM (2019) Depressive symptoms may increase the risk of the future development of freezing of gait in patients with Parkinson’s disease: findings from a 5-year prospective study. Parkinsonism Relat Disord 60:98–104PubMedCrossRef
50.
Zurück zum Zitat Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M et al (2001) Freezing of gait in PD prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721PubMedCrossRef Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M et al (2001) Freezing of gait in PD prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721PubMedCrossRef
51.
Zurück zum Zitat Giladi N, Treves TA, Simon ES, Shabtai H, Orlov Y, Kandinov B et al (2002) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm 108(1):53–61CrossRef Giladi N, Treves TA, Simon ES, Shabtai H, Orlov Y, Kandinov B et al (2002) Freezing of gait in patients with advanced Parkinson’s disease. J Neural Transm 108(1):53–61CrossRef
52.
Zurück zum Zitat Forsaa EB, Larsen JP, Wentzel-Larsen T, Alves G (2015) A 12-year population-based study of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 21(3):254–258PubMedCrossRef Forsaa EB, Larsen JP, Wentzel-Larsen T, Alves G (2015) A 12-year population-based study of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 21(3):254–258PubMedCrossRef
53.
Zurück zum Zitat Ehgoetz Martens KA, Lukasik EL, Georgiades MJ, Gilat M, Hall JM, Walton CC et al (2018) Predicting the onset of freezing of gait: a longitudinal study. Mov Disord 33(1):128–135PubMedCrossRef Ehgoetz Martens KA, Lukasik EL, Georgiades MJ, Gilat M, Hall JM, Walton CC et al (2018) Predicting the onset of freezing of gait: a longitudinal study. Mov Disord 33(1):128–135PubMedCrossRef
54.
Zurück zum Zitat Factor SA, Steenland NK, Higgins DS, Molho ES, Kay DM, Montimurro J et al (2011) Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry 82(5):564–568PubMedCrossRef Factor SA, Steenland NK, Higgins DS, Molho ES, Kay DM, Montimurro J et al (2011) Postural instability/gait disturbance in Parkinson’s disease has distinct subtypes: an exploratory analysis. J Neurol Neurosurg Psychiatry 82(5):564–568PubMedCrossRef
55.
Zurück zum Zitat Perez-Lloret S, Negre-Pages L, Damier P, Delval A, Derkinderen P, Destée A et al (2014) Prevalence, determinants, and effect on quality of life of freezing of gait in Parkinson disease. JAMA Neurol 71(7):884PubMedCrossRef Perez-Lloret S, Negre-Pages L, Damier P, Delval A, Derkinderen P, Destée A et al (2014) Prevalence, determinants, and effect on quality of life of freezing of gait in Parkinson disease. JAMA Neurol 71(7):884PubMedCrossRef
56.
Zurück zum Zitat Zhang H, Yin X, Ouyang Z, Chen J, Zhou S, Zhang C et al (2016) A prospective study of freezing of gait with early Parkinson disease in Chinese patients. Medicine (Baltimore) 95(26):e4056CrossRef Zhang H, Yin X, Ouyang Z, Chen J, Zhou S, Zhang C et al (2016) A prospective study of freezing of gait with early Parkinson disease in Chinese patients. Medicine (Baltimore) 95(26):e4056CrossRef
57.
Zurück zum Zitat Garcia-Ruiz PJ, Del Val J, Fernandez IM, Herranz A (2012) What factors influence motor complications in Parkinson disease?: A 10-year prospective study. Clin Neuropharmacol 35(1):1–5PubMedCrossRef Garcia-Ruiz PJ, Del Val J, Fernandez IM, Herranz A (2012) What factors influence motor complications in Parkinson disease?: A 10-year prospective study. Clin Neuropharmacol 35(1):1–5PubMedCrossRef
58.
Zurück zum Zitat Auyeung M, Tsoi TH, Mok V, Cheung CM, Lee CN, Li R et al (2012) Ten year survival and outcomes in a prospective cohort of new onset Chinese Parkinson’s disease patients. J Neurol Neurosurg Psychiatry 83(6):607–611PubMedCrossRef Auyeung M, Tsoi TH, Mok V, Cheung CM, Lee CN, Li R et al (2012) Ten year survival and outcomes in a prospective cohort of new onset Chinese Parkinson’s disease patients. J Neurol Neurosurg Psychiatry 83(6):607–611PubMedCrossRef
59.
Zurück zum Zitat Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M et al (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721PubMedCrossRef Giladi N, McDermott MP, Fahn S, Przedborski S, Jankovic J, Stern M et al (2001) Freezing of gait in PD: prospective assessment in the DATATOP cohort. Neurology 56(12):1712–1721PubMedCrossRef
60.
Zurück zum Zitat Sawada M, Wada-Isoe K, Hanajima R, Nakashima K (2019) Clinical features of freezing of gait in Parkinson’s disease patients. Brain Behav 9(4):e01244PubMedPubMedCentralCrossRef Sawada M, Wada-Isoe K, Hanajima R, Nakashima K (2019) Clinical features of freezing of gait in Parkinson’s disease patients. Brain Behav 9(4):e01244PubMedPubMedCentralCrossRef
61.
Zurück zum Zitat Maidan I, Plotnik M, Mirelman A, Weiss A, Giladi N, Hausdorff JM (2010) Heart rate changes during freezing of gait in patients with Parkinson’s disease. Mov Disord 25(14):2346–2354PubMedPubMedCentralCrossRef Maidan I, Plotnik M, Mirelman A, Weiss A, Giladi N, Hausdorff JM (2010) Heart rate changes during freezing of gait in patients with Parkinson’s disease. Mov Disord 25(14):2346–2354PubMedPubMedCentralCrossRef
63.
Zurück zum Zitat Lord S, Galna B, Coleman S, Burn D, Rochester L (2013) Mild depressive symptoms are associated with gait impairment in early Parkinson’s disease. Mov Disord 28(5):634–639PubMedCrossRef Lord S, Galna B, Coleman S, Burn D, Rochester L (2013) Mild depressive symptoms are associated with gait impairment in early Parkinson’s disease. Mov Disord 28(5):634–639PubMedCrossRef
64.
Zurück zum Zitat Giladi N, Hausdorff JM (2006) The role of mental function in the pathogenesis of freezing of gait in Parkinson’s disease. J Neurol Sci 248(1–2):173–176PubMedCrossRef Giladi N, Hausdorff JM (2006) The role of mental function in the pathogenesis of freezing of gait in Parkinson’s disease. J Neurol Sci 248(1–2):173–176PubMedCrossRef
65.
Zurück zum Zitat Amboni M, Cozzolino A, Longo K, Picillo M, Barone P (2008) Freezing of gait and executive functions in patients with Parkinson’s disease. Mov Disord 23(3):395–400PubMedCrossRef Amboni M, Cozzolino A, Longo K, Picillo M, Barone P (2008) Freezing of gait and executive functions in patients with Parkinson’s disease. Mov Disord 23(3):395–400PubMedCrossRef
66.
Zurück zum Zitat Nantel J, McDonald JC, Tan S, Bronte-Stewart H (2012) Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience 221:151–156PubMedCrossRef Nantel J, McDonald JC, Tan S, Bronte-Stewart H (2012) Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience 221:151–156PubMedCrossRef
67.
Zurück zum Zitat Abbott RD, Ross GW, White LR, Tanner CM, Masaki KH, Nelson JS et al (2005) Excessive daytime sleepiness and subsequent development of Parkinson disease. Neurology 65(9):1442–1446PubMedCrossRef Abbott RD, Ross GW, White LR, Tanner CM, Masaki KH, Nelson JS et al (2005) Excessive daytime sleepiness and subsequent development of Parkinson disease. Neurology 65(9):1442–1446PubMedCrossRef
68.
Zurück zum Zitat Stewart J, Bachman G, Cooper C, Liu L, Ancoli-Israel S, Alibiglou L (2018) Circadian dysfunction and fluctuations in gait initiation impairment in Parkinson’s disease. Exp Brain Res 236(3):655–664PubMedCrossRef Stewart J, Bachman G, Cooper C, Liu L, Ancoli-Israel S, Alibiglou L (2018) Circadian dysfunction and fluctuations in gait initiation impairment in Parkinson’s disease. Exp Brain Res 236(3):655–664PubMedCrossRef
69.
Zurück zum Zitat Tang X, Yu L, Yang J, Guo W, Liu Y, Xu Y et al (2021) Association of sleep disturbance and freezing of gait in Parkinson disease: prevention/delay implications. J Clin Sleep Med 17(4):779–789PubMedPubMedCentralCrossRef Tang X, Yu L, Yang J, Guo W, Liu Y, Xu Y et al (2021) Association of sleep disturbance and freezing of gait in Parkinson disease: prevention/delay implications. J Clin Sleep Med 17(4):779–789PubMedPubMedCentralCrossRef
70.
Zurück zum Zitat Ou R, Wei Q, Cao B, Song W, Hou Y, Liu H et al (2018) Predictors of freezing of gait in Chinese patients with Parkinson’s disease. Brain Behav 8(3):e00931PubMedPubMedCentralCrossRef Ou R, Wei Q, Cao B, Song W, Hou Y, Liu H et al (2018) Predictors of freezing of gait in Chinese patients with Parkinson’s disease. Brain Behav 8(3):e00931PubMedPubMedCentralCrossRef
71.
Zurück zum Zitat Long K, Wan C, Xiang Y, Liu J, Xu Q, Sun Q et al (2020) Study on the clinical features of Parkinson’s disease with probable rapid eye movement sleep behavior disorder. Front Neurol 11:979PubMedPubMedCentralCrossRef Long K, Wan C, Xiang Y, Liu J, Xu Q, Sun Q et al (2020) Study on the clinical features of Parkinson’s disease with probable rapid eye movement sleep behavior disorder. Front Neurol 11:979PubMedPubMedCentralCrossRef
72.
Zurück zum Zitat Videnovic A, Marlin C, Alibiglou L, Planetta PJ, Vaillancourt DE, MacKinnon (2013) Increased REM sleep without atonia in Parkinson disease with freezing of gait. Neurology 81:1030–1035PubMedPubMedCentralCrossRef Videnovic A, Marlin C, Alibiglou L, Planetta PJ, Vaillancourt DE, MacKinnon (2013) Increased REM sleep without atonia in Parkinson disease with freezing of gait. Neurology 81:1030–1035PubMedPubMedCentralCrossRef
73.
Zurück zum Zitat Kotagal V, Albin RL, Muller ML, Koeppe RA, Chervin RD, Frey KA et al (2012) Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 71(4):560–568PubMedPubMedCentralCrossRef Kotagal V, Albin RL, Muller ML, Koeppe RA, Chervin RD, Frey KA et al (2012) Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. Ann Neurol 71(4):560–568PubMedPubMedCentralCrossRef
74.
Zurück zum Zitat Fox SH, Chuang R, Brotchie JM (2009) Serotonin and Parkinson’s disease: on movement, mood, and madness. Mov Disord 24(9):1255–1266PubMedCrossRef Fox SH, Chuang R, Brotchie JM (2009) Serotonin and Parkinson’s disease: on movement, mood, and madness. Mov Disord 24(9):1255–1266PubMedCrossRef
75.
Zurück zum Zitat Prinz A, Selesnew LM, Liss B, Roeper J, Carlsson T (2013) Increased excitability in serotonin neurons in the dorsal raphe nucleus in the 6-OHDA mouse model of Parkinson’s disease. Exp Neurol 248:236–245PubMedCrossRef Prinz A, Selesnew LM, Liss B, Roeper J, Carlsson T (2013) Increased excitability in serotonin neurons in the dorsal raphe nucleus in the 6-OHDA mouse model of Parkinson’s disease. Exp Neurol 248:236–245PubMedCrossRef
76.
Zurück zum Zitat Albin RL, Koeppe RA, Bohnen NI, Wernette K, Kilbourn MA, Frey KA (2007) Spared caudal brainstem SERT binding in early Parkinson’s disease. J Cereb Blood Flow Metab 28(3):441–444PubMedCrossRef Albin RL, Koeppe RA, Bohnen NI, Wernette K, Kilbourn MA, Frey KA (2007) Spared caudal brainstem SERT binding in early Parkinson’s disease. J Cereb Blood Flow Metab 28(3):441–444PubMedCrossRef
77.
Zurück zum Zitat Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J (2009) Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol 120(12):2040–2054PubMedPubMedCentralCrossRef Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J (2009) Motoneuron excitability: the importance of neuromodulatory inputs. Clin Neurophysiol 120(12):2040–2054PubMedPubMedCentralCrossRef
78.
Zurück zum Zitat Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10(8):734–744PubMedPubMedCentralCrossRef Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A (2011) Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 10(8):734–744PubMedPubMedCentralCrossRef
79.
Zurück zum Zitat Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11):856–869PubMedCrossRef Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11):856–869PubMedCrossRef
80.
Zurück zum Zitat Brugger F, Wegener R, Walch J, Galovic M, Hagele-Link S, Bohlhalter S et al (2020) Altered activation and connectivity of the supplementary motor cortex at motor initiation in Parkinson’s disease patients with freezing. Clin Neurophysiol 131(9):2171–2180PubMedCrossRef Brugger F, Wegener R, Walch J, Galovic M, Hagele-Link S, Bohlhalter S et al (2020) Altered activation and connectivity of the supplementary motor cortex at motor initiation in Parkinson’s disease patients with freezing. Clin Neurophysiol 131(9):2171–2180PubMedCrossRef
81.
Zurück zum Zitat Nutt JG, Marsden CD, Thompson PD (1993) Human walking and higher-level gait disorders, particularly in the elderly. Neurology 43(2):268–279PubMedCrossRef Nutt JG, Marsden CD, Thompson PD (1993) Human walking and higher-level gait disorders, particularly in the elderly. Neurology 43(2):268–279PubMedCrossRef
82.
Zurück zum Zitat Shine JM, Naismith SL, Lewis SJ (2013) The differential yet concurrent contributions of motor, cognitive and affective disturbance to freezing of gait in Parkinson’s disease. Clin Neurol Neurosurg 115(5):542–545PubMedCrossRef Shine JM, Naismith SL, Lewis SJ (2013) The differential yet concurrent contributions of motor, cognitive and affective disturbance to freezing of gait in Parkinson’s disease. Clin Neurol Neurosurg 115(5):542–545PubMedCrossRef
83.
Zurück zum Zitat Pietracupa S, Suppa A, Upadhyay N, Gianni C, Grillea G, Leodori G et al (2018) Freezing of gait in Parkinson’s disease: gray and white matter abnormalities. J Neurol 265(1):52–62PubMedCrossRef Pietracupa S, Suppa A, Upadhyay N, Gianni C, Grillea G, Leodori G et al (2018) Freezing of gait in Parkinson’s disease: gray and white matter abnormalities. J Neurol 265(1):52–62PubMedCrossRef
84.
85.
Zurück zum Zitat Nieuwboer A, Giladi N (2013) Characterising freezing of gait in Parkinson’s disease: models of an episodic. Mov Disord 28(11):1509–1519PubMedCrossRef Nieuwboer A, Giladi N (2013) Characterising freezing of gait in Parkinson’s disease: models of an episodic. Mov Disord 28(11):1509–1519PubMedCrossRef
Metadaten
Titel
Associated factors and abnormal dorsal raphe nucleus connectivity patterns of freezing of gait in Parkinson’s disease
verfasst von
Lingling Lv
Hainan Zhang
Xuling Tan
Zhe Long
Lixia Qin
Rongrong Bai
Qile Xiao
Ziwei Wu
Shenglan Hu
Changlian Tan
Haiyan Liao
Weiqian Yan
Beisha Tang
Feng Ren
Chunyu Wang
Publikationsdatum
06.08.2022
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Neurology / Ausgabe 12/2022
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-022-11294-6

Weitere Artikel der Ausgabe 12/2022

Journal of Neurology 12/2022 Zur Ausgabe

Pioneers in Neurology

Josef Breuer (1842–1925)

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Hirnblutung unter DOAK und VKA ähnlich bedrohlich

17.05.2024 Direkte orale Antikoagulanzien Nachrichten

Kommt es zu einer nichttraumatischen Hirnblutung, spielt es keine große Rolle, ob die Betroffenen zuvor direkt wirksame orale Antikoagulanzien oder Marcumar bekommen haben: Die Prognose ist ähnlich schlecht.

Thrombektomie auch bei großen Infarkten von Vorteil

16.05.2024 Ischämischer Schlaganfall Nachrichten

Auch ein sehr ausgedehnter ischämischer Schlaganfall scheint an sich kein Grund zu sein, von einer mechanischen Thrombektomie abzusehen. Dafür spricht die LASTE-Studie, an der Patienten und Patientinnen mit einem ASPECTS von maximal 5 beteiligt waren.

Schwindelursache: Massagepistole lässt Otholiten tanzen

14.05.2024 Benigner Lagerungsschwindel Nachrichten

Wenn jüngere Menschen über ständig rezidivierenden Lagerungsschwindel klagen, könnte eine Massagepistole der Auslöser sein. In JAMA Otolaryngology warnt ein Team vor der Anwendung hochpotenter Geräte im Bereich des Nackens.

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Viertel reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.