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Dysphagia

pp 1–8 | Cite as

Alteration of Brain Functional Connectivity in Parkinson’s Disease Patients with Dysphagia

  • Jixiang Gao
  • Xiaojun Guan
  • Zhidong Cen
  • You Chen
  • Xueping Ding
  • Yuting Lou
  • Sheng Wu
  • Bo Wang
  • Zhiyuan Ouyang
  • Min Xuan
  • Quanquan Gu
  • Xiaojun Xu
  • Peiyu Huang
  • Minming Zhang
  • Wei LuoEmail author
Original Article
  • 117 Downloads

Abstract

Dysphagia is a common non-primary symptom of patients with Parkinson’s disease. The aim of this study is to investigate the underlying alterations of brain functional connectivity in Parkinson’s disease patients with dysphagia by resting-state functional magnetic resonance imaging. We recruited 13 Parkinson’s disease patients with dysphagia and ten patients without dysphagia, diagnosed by videofluoroscopic study of swallowing. Another 13 age and sex-matched healthy subjects were recruited. Eigenvector centrality mapping was computed to identify functional connectivity alterations among these groups. Parkinson’s disease patients with dysphagia had significantly increased functional connectivity in the cerebellum, left premotor cortex, the supplementary motor area, the primary motor cortex, right temporal pole of superior temporal gyrus, inferior frontal gyrus, anterior cingulate cortex and insula, compared with patients without dysphagia. This study suggests that functional connectivity changes in swallowing-related cortexes might contribute to the occurrence of dysphagia in Parkinson’s disease patients.

Keywords

Parkinson’s disease Dysphagia Functional connectivity Videofluoroscopic study of swallowing Deglutition Deglutition disorders 

Notes

Acknowledgments

The authors thank all the Parkinson’s disease patients and the normal controls who participated in our research.

Authors Contributions

JG designed the study, performed neurological evaluations, statistical analyses, and wrote the first draft. XG performed rsfMRI image preprocessing, statistical analyses and the review and critique of the manuscript. ZC, YC, XD and YL conducted VFSS data acquisition, neurological evaluations and the review and critique of the manuscript. SW, BW and ZO participated in subjects’ collection, VFSS data acquisition and neurological evaluations. MX, QG, XX, PH and MZ helped rsfMRI preprocessing. WL conceived of and organized the research project, participated in the neurological evaluations, and the review and critique of the manuscript.

Funding

This study was supported by the Science Technology Department of Zhejiang Province (Grant No. 2018C03G1121039), the Fundamental Research Funds for the Central Universities (Grant No. 2018FZA118) and the 13th Five-year Plan for National Key Research and Development Program of China (Grant No. 2016YFC1306600).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

455_2019_10015_MOESM1_ESM.docx (86 kb)
Supplementary material 1 (DOCX 86 kb)

References

  1. 1.
    Pflug C, Bihler M, Emich K. Critical dysphagia is common in Parkinson disease and occurs even in early stages: a prospective cohort study. Dysphagia. 2018;33(1):41–50.CrossRefGoogle Scholar
  2. 2.
    Costa MM. Videofluoroscopy: the gold standard exam for studying swallowing and its dysfunction. Arq Gastroenterol. 2010;47(4):327–8.CrossRefGoogle Scholar
  3. 3.
    Michou E, Hamdy S. Dysphagia in Parkinson’s disease: a therapeutic challenge? Expert Rev Neurother. 2010;10(6):875–8.CrossRefGoogle Scholar
  4. 4.
    Suttrup I, Warnecke T. Dysphagia in Parkinson’s disease. Dysphagia. 2016;31(1):24–32.CrossRefGoogle Scholar
  5. 5.
    Kikuchi A, Baba T, Hasegawa T, et al. Hypometabolism in the supplementary and anterior cingulate cortices is related to dysphagia in Parkinson’s disease: a cross-sectional and 3-year longitudinal cohort study. BMJ Open. 2013;3(3):e002249.CrossRefGoogle Scholar
  6. 6.
    Suntrup S, Teismann I, Bejer J, et al. Evidence for adaptive cortical changes in swallowing in Parkinson’s disease. Brain. 2013;136(3):726–38.CrossRefGoogle Scholar
  7. 7.
    Lohmann G, Margulies DS, Horstmann A, et al. Eigenvector centrality mapping for analyzing connectivity patterns in fMRI data of the human brain. PLoS ONE. 2010;5(4):e10232.CrossRefGoogle Scholar
  8. 8.
    Jech R, Mueller K, Schroeter ML, et al. Levodopa increases functional connectivity in the cerebellum and brainstem in Parkinson’s disease. Brain. 2013;136(7):e234.CrossRefGoogle Scholar
  9. 9.
    Zhang MY, Katzman R, Salmon D, et al. The prevalence of dementia and Alzheimer’s disease in Shanghai, China: impact of age, gender, and education. Ann Neurol. 1990;27(4):428–37.CrossRefGoogle Scholar
  10. 10.
    Katzman R, Zhang MY, Ouang-Ya-Qu, et al. A chinese version of the mini-mental state examination; impact of illiteracy in a shanghai dementia survey. J Clin Epidemiol. 1988;41(10):971–8.CrossRefGoogle Scholar
  11. 11.
    Ding X, Gao J, Xie C, et al. Prevalance and clinical correlation of dysphagia in Parkinson disease: a study on Chinese patients. Eur J Clin Nutr. 2018;72(1):82–6.CrossRefGoogle Scholar
  12. 12.
    Wink AM, de Munck JC, van der Werf YD, et al. Fast eigenvector centrality mapping of voxel-wise connectivity in functional magnetic resonance imaging: implementation, validation, and interpretation. Brain Connect. 2012;2(5):265–74.CrossRefGoogle Scholar
  13. 13.
    Hamdy S, Rothwell J, Brooks D, et al. Identification of the cerebral loci processing human swallowing with H2(15) O PET activation. J Neurophysiol. 1999;81(4):1917–26.CrossRefGoogle Scholar
  14. 14.
    Humbert IA, Robbins J. Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia. 2007;22(3):266–75.CrossRefGoogle Scholar
  15. 15.
    Li S, Luo C, Yu B, et al. Functional magnetic resonance imaging study on dysphagia after unilateral hemispheric stroke: a preliminary study. J Neurol Neurosurg Psychiatry. 2009;80(12):1320–9.CrossRefGoogle Scholar
  16. 16.
    Liu L, Xiao Y, Zhang W, et al. Functional changes of neural circuits in stroke patients with dysphagia: a meta-analysis. J Evid Based Med. 2017;10(3):189–95.CrossRefGoogle Scholar
  17. 17.
    Mosier K, Bereznaya I. Parallel cortical networks for voli- tional control of swallowing in humans. Exp Brain Res. 2001;140:280–9.CrossRefGoogle Scholar
  18. 18.
    Rangarathnam B, Kamarunas E, McCullough GH. Role of cerebellum in deglutition and deglutition disorders. Cerebellum. 2014;13(6):767–76.CrossRefGoogle Scholar
  19. 19.
    Vasant DH, Michou E, Mistry S, et al. High-frequency focal repetitive cerebellar stimulation induces prolonged increases in human pharyngeal motor cortex excitability. J Physiol. 2015;593(22):4963–77.CrossRefGoogle Scholar
  20. 20.
    Geng D, Li YX, Zee CS. Magnetic resonance imaging-based volumetric analysis of basal ganglia nuclei and substantia nigra in patients with Parkinson’s disease. Neurosurgery. 2006;58(2):256–62.CrossRefGoogle Scholar
  21. 21.
    Wang J, Jiang YP, Xiang JD, et al. The significance of 18F-FP- CIT dopamine transporter PET imaging in early diagnosis of Parkinson’s disease. Chin J Nucl Med. 2003;23(4):216–8.Google Scholar
  22. 22.
    Lou Y, Huang P, Li D, et al. Altered brain network centrality in depressed Parkinson’s disease patients. Mov Disord. 2015;30(13):1777–84.CrossRefGoogle Scholar
  23. 23.
    de Schipper LJ, Hafkemeijer A, van der Grond J, et al. Altered whole-brain and network-based functional connectivity in Parkinson’s disease. Front Neurol. 2018;9:419.CrossRefGoogle Scholar
  24. 24.
    Mueller K, Jech R, Růžička F, Holiga Š, et al. Brain connectivity changes when comparing effects of subthalamic deep brain stimulation with levodopa treatment in Parkinson’s disease. Neuroimage Clin. 2018;19:1025–35.CrossRefGoogle Scholar
  25. 25.
    Lewis SJG, Dove A, Robbins TW, et al. Cognitive impairments in early Parkinson’s disease are accompanied by reductions in activity in frontostriatal neural circuitry. J Neurosci. 2003;23:6351–6.CrossRefGoogle Scholar
  26. 26.
    Vossel S, Geng JJ, Fink GR. Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist. 2014;20:150–9.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Jixiang Gao
    • 1
    • 2
  • Xiaojun Guan
    • 3
  • Zhidong Cen
    • 1
  • You Chen
    • 1
  • Xueping Ding
    • 4
  • Yuting Lou
    • 5
  • Sheng Wu
    • 1
  • Bo Wang
    • 1
  • Zhiyuan Ouyang
    • 1
  • Min Xuan
    • 3
  • Quanquan Gu
    • 3
  • Xiaojun Xu
    • 3
  • Peiyu Huang
    • 3
  • Minming Zhang
    • 3
  • Wei Luo
    • 1
    Email author
  1. 1.Department of NeurologyThe Second Affiliated Hospital, Zhejiang University School of MedicineHangzhouChina
  2. 2.Department of NeurologyHangzhou Hospital of Traditional Chinese MedicineHangzhouChina
  3. 3.Department of RadiologyThe Second Affiliated Hospital, Zhejiang University School of MedicineHangzhouChina
  4. 4.Department of NeurologyPeople’s Hospital of HainingHainingChina
  5. 5.Department of PediatricsThe Second Affiliated Hospital, Zhejiang University School of MedicineHangzhouChina

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