nach oben

Journal of Neurology

Erschienen in:

29.06.2023 | Original Communication

Study of the relationship between onset lateralization and hemispheric white matter asymmetry in Parkinson's disease

verfasst von: Yuxia Zhu, Sichen Li, Xiaohui Da, Hongyu Lai, Changhong Tan, Xi Liu, Fen Deng, Lifen Chen

Erschienen in: Journal of Neurology | Ausgabe 10/2023

Einloggen, um Zugang zu erhalten

Abstract

Background

Parkinson's disease (PD) is characterized by a lateralized onset, but its cause and mechanism are still unclear.

Methods

Obtaining diffusion tensor imaging (DTI) data from the Parkinson’s Progression Markers Initiative (PPMI). Tract-based spatial statistics analysis and region-of-interest-based analysis were performed to evaluate the white matter (WM) asymmetry using original DTI parameters, Z Score normalized parameters, or the asymmetry index (AI). Hierarchical cluster analysis and least absolute shrinkage and selection operator regression were performed to construct predictive models for predicting the PD onset side. DTI data from The Second Affiliated Hospital of Chongqing Medical University were obtained for external validation of the prediction model.

Results

118 PD patients and 69 healthy controls (HC) from PPMI were included. Right-onset PD patients presented more asymmetric areas than left-onset PD patients. The inferior cerebellar peduncle (ICP), superior cerebellar peduncle (SCP), external capsule (EC), cingulate gyrus (CG), superior fronto-occipital fasciculus (SFO), uncinate fasciculus (UNC), and tapetum (TAP) showed significant asymmetry in left-onset and right-onset PD patients. An onset-side-specific pattern of WM alterations exists in PD patients, and a prediction model was constructed. The predicting models based on AI and ΔZ Score presented favorable efficacy in predicting PD onset side by external validation in 26 PD patients and 16 HCs from our hospital.

Conclusions

Right-onset PD patients may have more severe WM damage than left-onset PD patients. WM asymmetry in ICP, SCP, EC, CG, SFO, UNC, and TAP may predict PD onset side. Imbalances in the WM network may underlie the mechanism of lateralized onset in PD.

Nur mit Berechtigung zugänglich

Miller DB, O’Callaghan JP (2015) Biomarkers of Parkinson’s disease: Present and future. Metabolism 64:S40–S46. https://doi.org/10.1016/j.metabol.2014.10.030CrossRefPubMed

Wang J, Yang QX, Sun X et al (2015) MRI evaluation of asymmetry of nigrostriatal damage in the early stage of early-onset Parkinson’s disease. Parkinsonism Relat Disord 21:590–596. https://doi.org/10.1016/j.parkreldis.2015.03.012CrossRefPubMed

Djaldetti R, Ziv I, Melamed E (2006) The mystery of motor asymmetry in Parkinson’s disease. The Lancet Neurology 5:796–802. https://doi.org/10.1016/S1474-4422(06)70549-XCrossRefPubMed

Postuma RB, Berg D, Stern M et al (2015) MDS clinical diagnostic criteria for Parkinson’s disease: MDS-PD Clinical Diagnostic Criteria. Mov Disord 30:1591–1601. https://doi.org/10.1002/mds.26424CrossRefPubMed

Özekmekçi S, Benbir G, Özdogan FY et al (2007) Hemihypomimia, a rare persistent sign in Parkinson’s disease: follow up of 11 patients. J Neurol 254:347–350. https://doi.org/10.1007/s00415-006-0372-zCrossRefPubMed

Guerra-Hiraldo JD, López-Jiménez A, Gasca-Salas C et al (2023) Hemihypomimia in Parkinson’s disease: an under-recognized clinical sign? J Neurol 270:548–551. https://doi.org/10.1007/s00415-022-11292-8CrossRefPubMed

Djaldetti R, Shifrin A, Rogowski Z et al (2004) Quantitative measurement of pain sensation in patients with Parkinson disease. Neurology 62:2171–2175. https://doi.org/10.1212/01.WNL.0000130455.38550.9DCrossRefPubMed

Fusina S, Conte S, Bertolasi L et al (1999) Sympathetic skin response asymmetry in early stage idiopathic Parkinson’s disease. Clin Neurophysiol 110:358–366. https://doi.org/10.1016/S1388-2457(98)00012-1CrossRefPubMed

Quinn NP, Lang AE, Koller WC, Marsden CD (1986) PAINFUL PARKINSON’S DISEASE. The Lancet 327:1366–1369. https://doi.org/10.1016/S0140-6736(86)91674-0CrossRef

10.

Snider SR, Fahn S, Isgreen WP, Cote LJ (1976) Primary sensory symptoms in parkinsonism. Neurology 26:423–429. https://doi.org/10.1212/wnl.26.5.423CrossRefPubMed

11.

Levin J, Kurz A, Arzberger T et al (2016) The Differential Diagnosis and Treatment of Atypical Parkinsonism. Dtsch Arztebl Int. https://doi.org/10.3238/arztebl.2016.0061CrossRefPubMedPubMedCentral

12.

Ham JH, Lee JJ, Kim JS et al (2015) Is dominant-side onset associated with a better motor compensation in Parkinson’s disease? Mov Disord 30:1921–1925. https://doi.org/10.1002/mds.26418CrossRefPubMed

13.

Sawle GV, Playford ED, Brooks DJ et al (1993) Asymmetrical pre-synaptic and post-synaptic changes in the striatal dopamine projection in dopa naïve parkinsonism: diagnostic implications of the D2 receptor status. Brain 116:853–867. https://doi.org/10.1093/brain/116.4.853CrossRefPubMed

14.

Pelizzari L, Di Tella S, Laganà MM et al (2020) White matter alterations in early Parkinson’s disease: role of motor symptom lateralization. Neurol Sci 41:357–364. https://doi.org/10.1007/s10072-019-04084-yCrossRefPubMed

15.

Marek K, Jennings D, Lasch S et al (2011) The Parkinson Progression Marker Initiative (PPMI). Prog Neurobiol 95:629–635. https://doi.org/10.1016/j.pneurobio.2011.09.005CrossRefPubMedCentral

16.

Jenkinson M, Beckmann CF, Behrens TEJ et al (2012) FSL NeuroImage 62:782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015CrossRefPubMed

17.

Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505. https://doi.org/10.1016/j.neuroimage.2006.02.024CrossRefPubMed

18.

Winkler AM, Ridgway GR, Webster MA et al (2014) Permutation inference for the general linear model. Neuroimage 92:381–397. https://doi.org/10.1016/j.neuroimage.2014.01.060CrossRefPubMed

19.

Mori S, Oishi K, Jiang H et al (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40:570–582. https://doi.org/10.1016/j.neuroimage.2007.12.035CrossRefPubMed

20.

Boscolo Galazzo I, Mattoli MV, Pizzini FB, et al (2016) Cerebral metabolism and perfusion in MR-negative individuals with refractory focal epilepsy assessed by simultaneous acquisition of 18 F-FDG PET and arterial spin labeling. NeuroImage: Clinical 11:648–657. https://doi.org/10.1016/j.nicl.2016.04.005

21.

Carper RA, Treiber JM, DeJesus SY, Müller R-A (2016) Reduced hemispheric asymmetry of white matter microstructure in autism spectrum disorder. J Am Acad Child Adolesc Psychiatry 55:1073–1080. https://doi.org/10.1016/j.jaac.2016.09.491CrossRefPubMedPubMedCentral

22.

Riederer P, Sian-Hülsmann J (2012) The significance of neuronal lateralisation in Parkinson’s disease. J Neural Transm 119:953–962. https://doi.org/10.1007/s00702-012-0775-1CrossRefPubMed

23.

Baumann CR, Held U, Valko PO et al (2014) Body side and predominant motor features at the onset of Parkinson’s disease are linked to motor and nonmotor progression: Predictors of PD Motor and Nonmotor Outcomes. Mov Disord 29:207–213. https://doi.org/10.1002/mds.25650CrossRefPubMed

24.

Munhoz RP, Espay AJ, Morgante F et al (2013) Long-duration Parkinson’s disease: Role of lateralization of motor features. Parkinsonism Relat Disord 19:77–80. https://doi.org/10.1016/j.parkreldis.2012.07.008CrossRefPubMed

25.

Frazzitta G, Ferrazzoli D, Maestri R, et al (2015) Differences in Muscle Strength in Parkinsonian Patients Affected on the Right and Left Side. PLoS ONE 10:e0121251. https://doi.org/10.1371/journal.pone.0121251

26.

Rektor I, Svátková A, Vojtíšek L, et al (2018) White matter alterations in Parkinson’s disease with normal cognition precede grey matter atrophy. PLoS ONE 13:e0187939. https://doi.org/10.1371/journal.pone.0187939

27.

Scherfler C, Seppi K, Mair KJ et al (2012) Left hemispheric predominance of nigrostriatal dysfunction in Parkinson’s disease. Brain 135:3348–3354. https://doi.org/10.1093/brain/aws253CrossRefPubMed

28.

Iranzo A, Stefani A, Niñerola-Baizan A et al (2020) Left-hemispheric predominance of nigrostriatal deficit in isolated REM sleep behavior disorder. Neurology 94:e1605–e1613. https://doi.org/10.1212/WNL.0000000000009246CrossRefPubMed

29.

Kim JS, Yang J, Lee J et al (2014) Topographic pattern of cortical thinning with consideration of motor laterality in Parkinson disease. Parkinsonism Relat Disord 20:1186–1190. https://doi.org/10.1016/j.parkreldis.2014.08.021CrossRefPubMed

30.

Thiebaut de Schotten M, Forkel SJ (2022) The emergent properties of the connected brain. Science 378:505–510. https://doi.org/10.1126/science.abq2591CrossRefPubMed

31.

Standring S (2008) Gray’s Anatomy, 40th edn. Churchill Livingstone, London

32.

Zhong Y, Liu H, Liu G, et al (2022) A review on pathology, mechanism, and therapy for cerebellum and tremor in Parkinson’s disease. npj Parkinsons Dis 8:82. https://doi.org/10.1038/s41531-022-00347-2

33.

Ogawa T, Hatano T, Kamagata K et al (2021) White matter alterations in Parkinson’s disease with levodopa-induced dyskinesia. Parkinsonism Relat Disord 90:8–14. https://doi.org/10.1016/j.parkreldis.2021.07.021CrossRefPubMed

34.

Shen Q, Liu Y, Guo J et al (2022) Impaired white matter microstructure associated with severe depressive symptoms in patients with PD. Brain Imaging Behav 16:169–175. https://doi.org/10.1007/s11682-021-00488-7CrossRefPubMed

35.

Uhr L, Tsolaki E, Pouratian N (2022) Diffusion tensor imaging correlates of depressive symptoms in Parkinson disease. J of Comparative Neurology 530:1729–1738. https://doi.org/10.1002/cne.25310CrossRef

36.

Takeshige-Amano H, Hatano T, Kamagata K et al (2022) White matter microstructures in Parkinson’s disease with and without impulse control behaviors. Ann Clin Transl Neurol 9:253–263. https://doi.org/10.1002/acn3.51504CrossRefPubMedPubMedCentral

37.

Wang J, Zhang F, Zhao C, et al (2020) Investigation of local white matter abnormality in Parkinson’s disease by using an automatic fiber tract parcellation. Behavioural Brain Research 394:112805. https://doi.org/10.1016/j.bbr.2020.112805

38.

Lucas-Jiménez O, Díez-Cirarda M, Ojedaa N et al (2015) Verbal memory in parkinson’s disease: a combined DTI and fMRI study. J Parkinsons Dis 5:793–804. https://doi.org/10.3233/jpd-150623CrossRefPubMedPubMedCentral

39.

Di Tella S, Baglio F, Pelizzari L, et al (2020) Uncinate fasciculus and word selection processing in Parkinson’s disease. Neuropsychologia 146:107504. https://doi.org/10.1016/j.neuropsychologia.2020.107504

40.

Bubb EJ, Metzler-Baddeley C, Aggleton JP (2018) The cingulum bundle: anatomy, function, and dysfunction. Neurosci Biobehav Rev 92:104–127. https://doi.org/10.1016/j.neubiorev.2018.05.008CrossRefPubMedPubMedCentral

41.

Dalgleish T (2004) The emotional brain. Nat Rev Neurosci 5:583–589. https://doi.org/10.1038/nrn1432CrossRefPubMed

42.

Kantarci K, Senjem ML, Avula R et al (2011) Diffusion tensor imaging and cognitive function in older adults with no dementia. Neurology 77:26–34. https://doi.org/10.1212/WNL.0b013e31822313dcCrossRefPubMedPubMedCentral

43.

Aarsland D, Batzu L, Halliday GM et al (2021) Parkinson disease-associated cognitive impairment. Nat Rev Dis Primers 7:47. https://doi.org/10.1038/s41572-021-00280-3CrossRefPubMed

44.

Lally H, Hart AR, Bay AA et al (2020) Association between motor subtype and visuospatial and executive function in mild-moderate Parkinson disease. Arch Phys Med Rehabil 101:1580–1589. https://doi.org/10.1016/j.apmr.2020.05.018CrossRefPubMed

45.

Du J, Zhu H, Yu L, et al (2021) Multi-Dimensional Diffusion Tensor Imaging Biomarkers for Cognitive Decline From the Preclinical Stage: A Study of Post-stroke Small Vessel Disease. Front Neurol 12:687959. https://doi.org/10.3389/fneur.2021.687959

46.

Goldwaser EL, Du X, Adhikari BM et al (2022) Role of white matter microstructure in impulsive behavior. JNP 34:254–260. https://doi.org/10.1176/appi.neuropsych.21070167CrossRef

47.

Pu W, Shen X, Huang M et al (2020) Assessment of white matter lesions in Parkinson’s disease: voxel-based analysis and tract-based spatial statistics analysis of Parkinson’s disease with mild cognitive impairment. Curr Neurovasc Res 17:480–486. https://doi.org/10.2174/1567202617666200901181842CrossRefPubMed

48.

Chen L, Zeng X, Zhou S, et al (2022) Correlation Between Serum High-Sensitivity C-Reactive Protein, Tumor Necrosis Factor-Alpha, Serum Interleukin-6 and White Matter Integrity Before and After the Treatment of Drug-Naïve Patients With Major Depressive Disorder. Front Neurosci 16:948637. https://doi.org/10.3389/fnins.2022.948637

49.

Chen B, Akshita J, Han P et al (2020) Aberrancies of brain network structures in patients with anosmia. Brain Topogr 33:403–411. https://doi.org/10.1007/s10548-020-00769-2CrossRefPubMed

50.

Seppi K, Ray Chaudhuri K, Coelho M et al (2019) Update on treatments for nonmotor symptoms of Parkinson’s disease-an evidence-based medicine review. Mov Disord 34:180–198. https://doi.org/10.1002/mds.27602CrossRefPubMedPubMedCentral

51.

Gao C, Liu J, Tan Y, Chen S (2020) Freezing of gait in Parkinson’s disease: pathophysiology, risk factors and treatments. Transl Neurodegener 9:12. https://doi.org/10.1186/s40035-020-00191-5CrossRefPubMedPubMedCentral

52.

Chen L, Hu X, Ouyang L et al (2016) A systematic review and meta-analysis of tract-based spatial statistics studies regarding attention-deficit/hyperactivity disorder. Neurosci Biobehav Rev 68:838–847. https://doi.org/10.1016/j.neubiorev.2016.07.022CrossRefPubMed

53.

Mander BA, Zhu AH, Lindquist JR et al (2017) White matter structure in older adults moderates the benefit of sleep spindles on motor memory consolidation. J Neurosci 37:11675–11687. https://doi.org/10.1523/JNEUROSCI.3033-16.2017CrossRefPubMedPubMedCentral

54.

Rau Y-A, Wang S-M, Tournier J-D, et al (2019) A longitudinal fixel-based analysis of white matter alterations in patients with Parkinson’s disease. NeuroImage: Clinical 24:102098. https://doi.org/10.1016/j.nicl.2019.102098

55.

Fernández-Miranda JC, Rhoton AL, Kakizawa Y et al (2008) The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study: Laboratory investigation. JNS 108:764–774. https://doi.org/10.3171/JNS/2008/108/4/0764CrossRef

56.

Su W, Li K, Li C-M, et al (2021) Motor Symptom Lateralization Influences Cortico-Striatal Functional Connectivity in Parkinson’s Disease. Front Neurol 12:619631. https://doi.org/10.3389/fneur.2021.619631

57.

Gotts SJ, Jo HJ, Wallace GL et al (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci USA 110:E3435-3444. https://doi.org/10.1073/pnas.1302581110CrossRefPubMedPubMedCentral

58.

Di Tella S, Baglio F, Cabinio M et al (2018) Selection Processing in Noun and Verb Production in Left- and Right-Sided Parkinson’s Disease Patients. Front Psychol 9:1241. https://doi.org/10.3389/fpsyg.2018.01241CrossRefPubMedPubMedCentral

59.

Foster PS, Drago V, Crucian GP et al (2011) Anxiety and depression severity are related to right but not left onset Parkinson’s disease duration. J Neurol Sci 305:131–135. https://doi.org/10.1016/j.jns.2011.02.023CrossRefPubMed

60.

Verreyt N, Nys GMS, Santens P, Vingerhoets G (2011) Cognitive differences between patients with left-sided and right-sided Parkinson’s disease. A Review. Neuropsychol Rev 21:405–424. https://doi.org/10.1007/s11065-011-9182-xCrossRefPubMed

61.

Miller IN, Cronin-Golomb A (2010) Gender differences in Parkinson’s disease: clinical characteristics and cognition: gender differences in Parkinson’s disease. Mov Disord 25:2695–2703. https://doi.org/10.1002/mds.23388CrossRefPubMedPubMedCentral

62.

Bentivoglio AR, Lo Monaco MR, Liperoti R, et al (2021) Gender may be related to the side of the motor syndrome and cognition in idiopathic Parkinson’s disease. Neurologia (Engl Ed) 13:S0213–4853(21)00025–6. https://doi.org/10.1016/j.nrl.2021.01.009

63.

Adwani S, Yadav R, Kumar K et al (2016) Neuropsychological profile in early Parkinson′s disease: comparison between patients with right side onset versus left side onset of motor symptoms. Ann Indian Acad Neurol 19:74. https://doi.org/10.4103/0972-2327.167711CrossRefPubMedPubMedCentral

64.

Voruz P, Pierce J, Ahrweiller K et al (2022) Motor symptom asymmetry predicts non-motor outcome and quality of life following STN DBS in Parkinson’s disease. Sci Rep 12:3007. https://doi.org/10.1038/s41598-022-07026-5CrossRefPubMedPubMedCentral

65.

Bove F, Cavallieri F, Castrioto A, et al (2022) Does Motor Symptoms Asymmetry Predict Motor Outcome of Subthalamic Deep Brain Stimulation in Parkinson’s Disease Patients? Front Hum Neurosci 16:931858. https://doi.org/10.3389/fnhum.2022.931858

66.

Hershey T, Wu J, Weaver PM et al (2008) Unilateral vs. bilateral STN DBS effects on working memory and motor function in Parkinson disease. Exp Neurol 210:402–408. https://doi.org/10.1016/j.expneurol.2007.11.011CrossRefPubMed

Titel: Study of the relationship between onset lateralization and hemispheric white matter asymmetry in Parkinson's disease
verfasst von: Yuxia Zhu
Sichen Li
Xiaohui Da
Hongyu Lai
Changhong Tan
Xi Liu
Fen Deng
Lifen Chen
Publikationsdatum: 29.06.2023
Verlag: Springer Berlin Heidelberg
Erschienen in: Journal of Neurology / Ausgabe 10/2023
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-023-11849-1

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

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 Vierten reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Bluttest erkennt Parkinson schon zehn Jahre vor der Diagnose

10.05.2024 Parkinson-Krankheit Nachrichten

Ein Bluttest kann abnorm aggregiertes Alpha-Synuclein bei einigen Menschen schon zehn Jahre vor Beginn der motorischen Parkinsonsymptome nachweisen. Mit einem solchen Test lassen sich möglicherweise Prodromalstadien erfassen und die Betroffenen früher behandeln.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Wartezeit nicht kürzer, aber Arbeit flexibler

Psychotherapie Medizin aktuell

Fünf Jahren nach der Neugestaltung der Psychotherapie-Richtlinie wurden jetzt die Effekte der vorgenommenen Änderungen ausgewertet. Das Hauptziel der Novellierung war eine kürzere Wartezeit auf Therapieplätze. Dieses Ziel wurde nicht erreicht, es gab jedoch positive Auswirkungen auf andere Bereiche.

Update Neurologie

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

Newsletter bestellen

Klimawandel und Gesundheit: Was Sie in der Hausarztpraxis wissen müssen und tun können

Springer Medizin

Abstract

Background

Methods

Results

Conclusions

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 10/2023

Functional connectivity modifications in monoaminergic circuits occur in fatigued MS patients treated with fampridine and amantadine

Frailty in aneurysmal subarachnoid hemorrhage: the risk analysis index

Serum levels of neurofilament light chains in pediatric multiple sclerosis: a systematic review and meta-analysis

Sutton’s law applies to functional neurology

Establishing normative data for the evaluation of cognitive performance in Huntington’s disease considering the impact of gender, age, language, and education