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

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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.

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References

  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.

    Article  PubMed  Google Scholar 

  2. Costa MM. Videofluoroscopy: the gold standard exam for studying swallowing and its dysfunction. Arq Gastroenterol. 2010;47(4):327–8.

    Article  PubMed  Google Scholar 

  3. Michou E, Hamdy S. Dysphagia in Parkinson’s disease: a therapeutic challenge? Expert Rev Neurother. 2010;10(6):875–8.

    Article  PubMed  Google Scholar 

  4. Suttrup I, Warnecke T. Dysphagia in Parkinson’s disease. Dysphagia. 2016;31(1):24–32.

    Article  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  14. Humbert IA, Robbins J. Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia. 2007;22(3):266–75.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  17. Mosier K, Bereznaya I. Parallel cortical networks for voli- tional control of swallowing in humans. Exp Brain Res. 2001;140:280–9.

    Article  CAS  PubMed  Google Scholar 

  18. Rangarathnam B, Kamarunas E, McCullough GH. Role of cerebellum in deglutition and deglutition disorders. Cerebellum. 2014;13(6):767–76.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  26. Vossel S, Geng JJ, Fink GR. Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist. 2014;20:150–9.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

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

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).

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Author notes

  1. Jixiang Gao and Xiaojun Guan contributed equally to this work and should be considered co-first authors.

Authors and Affiliations

  1. Department of Neurology, The Second Affiliated Hospital, Zhejiang University School of Medicine, 88 Jiefang Road, Hangzhou, 310009, Zhejiang, China

    Jixiang Gao, Zhidong Cen, You Chen, Sheng Wu, Bo Wang, Zhiyuan Ouyang & Wei Luo

  2. Department of Neurology, Hangzhou Hospital of Traditional Chinese Medicine, Hangzhou, Zhejiang, China

    Jixiang Gao

  3. Department of Radiology, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China

    Xiaojun Guan, Min Xuan, Quanquan Gu, Xiaojun Xu, Peiyu Huang & Minming Zhang

  4. Department of Neurology, People’s Hospital of Haining, Haining, Zhejiang, China

    Xueping Ding

  5. Department of Pediatrics, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China

    Yuting Lou

Authors
  1. Jixiang Gao
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  2. Xiaojun Guan
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  3. Zhidong Cen
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  4. You Chen
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  6. Yuting Lou
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  7. Sheng Wu
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  8. Bo Wang
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  10. Min Xuan
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  11. Quanquan Gu
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  12. Xiaojun Xu
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  13. Peiyu Huang
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  14. Minming Zhang
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  15. Wei Luo
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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.

Corresponding author

Correspondence to Wei Luo.

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The authors declare that they have no conflict of interest.

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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.

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

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Gao, J., Guan, X., Cen, Z. et al. Alteration of Brain Functional Connectivity in Parkinson’s Disease Patients with Dysphagia. Dysphagia 34, 600–607 (2019). https://doi.org/10.1007/s00455-019-10015-y

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  • DOI: https://doi.org/10.1007/s00455-019-10015-y

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