ORIGINAL RESEARCH

Ultrasound imaging of vagus nerves in patients with Parkinson's disease

About authors

Research Center of Neurology, Moscow, Russia

Correspondence should be addressed: Andrey О. Chechetkin
Volokolamskoe shosse, 80, Moscow, 125367, Russia; moc.liamg@niktehcehcyerdna

About paper

Author contribution: Chechetkin AO — study design, acquisition of ultrasound imaging data, data interpretation, manuscript preparation; Moskalenko AN — clinical data acquisition, analysis and interpretation; Fedotova EYu, Illarioshkin SN — study design, manuscript editing.

Compliance with ethical standards: the study was approved by the Ethics Committee of the Research Center of Neurology (Protocol No. 2-6/20 dated March 18, 2020)

Received: 2021-10-25 Accepted: 2021-11-11 Published online: 2021-11-24
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  1. Poewe W, Seppi K, Tanner CM, Halliday GM, Brundin P, Volkmann J, et al. Parkinson disease. Nat Rev Dis Primers. 2017; 3 (1): 1–21. DOI: 10.1038/nrdp.2017.13.
  2. Klingelhoefer L, Reichmann H. Pathogenesis of Parkinson disease–the gutbrain axis and environmental factors. Nat Rev Neurol. 2015. 11; 625–36. DOI: 10.1038/nrneurol.2015.197.
  3. Hawkes CH, Del Tredici K, Braak H. Parkinson’s disease: a dualhit hypothesis. Neuropathol Appl Neurobiol. 2007; 33: 599–614. DOI: 10.1111/j.1365-2990.2007.00874.x.
  4. Horsager J, Walter U, Fedorova TD, Andersen KB, Skjærbæk C, Knudsen K, et al. Vagus Nerve Cross-Sectional Area in Patients With Parkinson's Disease-An Ultrasound CaseControl Study. Front Neurol. 2021; 12: 681413. DOI: 10.3389/ fneur.2021.681413.
  5. Del Tredici K, Braak H. Review: Sporadic Parkinson’s disease: development and distribution of α-synuclein pathology. Neuropathol Appl Neurobiol. 2016; 42: 33–50. DOI: 10.1111/ nan.12298.
  6. Svensson E, Horváth-Puhó E, Thomsen RW, Djurhuus JC, Pedersen L, Borghammer P, et al. Vagotomy and subsequent risk of Parkinson’s disease. Ann Neurol. 2015; 78: 522–29. DOI: 10.1002/ana.24448.
  7. Liu B, Fang F, Pedersen NL, Tillander A, Ludvigsson JF, Ekbom A, et al. Vagotomy and Parkinson disease: a Swedish register-based matchedcohort study. Neurology. 2017; 88: 1996–2002. DOI: 10.1212/WNL.0000000000 003961.
  8. Holmqvist S, Chutna O, Bousset L, Aldrin-Kirk P, Li W, Björklund T., et al. Direct evidence of Parkinson pathology spread from the gastrointestinal tract to the brain in rats. Acta Neuropathol. 2014; 128: 805–20. DOI: 10.1007/s00401-014-1343-6.
  9. Mu L, Sobotka S, Chen J, Su H, Sanders I, Adler C, et al. Alphasynuclein pathology and axonal degeneration of the peripheral motor nerves innervating pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol. 2013. 72; 119–29. DOI: 10.1097/NEN.0b013e3182 801cde.
  10. Nakamura K, Mori F, Tanji K, Miki Y, Toyoshima Y, Kakita A, et al. α-Synuclein pathology in the cranial and spinal nerves in Lewy body disease. Neuropathology. 2016; 36: 262–69. DOI: 10.1111/ neup. 12269.
  11. Gjerloff T, Fedorova T, Knudsen K, Munk O, Nahimi A, Jacobsen S, et al. Imaging acetylcholinesterase density in peripheral organs in Parkinson’s disease with 11C-donepezil PET. Brain. 2015; 138 (Pt 3): 653–63. DOI: 10.1093/brain/awu369.
  12. Fedorova T, Seidelin L, Knudsen K, Schacht A, Geday J, Pavese N, et al. Decreased intestinal acetylcholinesterase in early Parkinson disease: An (11)C-donepezil PET study. Neurology. 2017. 88: 775–81. DOI: 10.1212/WNL.0000000000003633.
  13. Grimm A, Décard B, Athanasopoulou I, Schweikert K, Sinnreich M, Axer H. Nerve ultrasound for differentiation between amyotrophic lateral sclerosis and multifocal motor neuropathy. J Neurol. 2015; 262: 870–80. DOI: 10.1007/s00415-015-7648-0.
  14. Hong M, Baek J, Kim D, Ha E, Choi W, Choi Y, et al. Spinal accessory nerve: ultrasound findings and correlations with neck lymph node levels. Ultraschall Med. 2016; 37: 487–91. DOI: 10.1055/s-0034-1385673.
  15. Tawfik E, Walker F, Cartwright M, El-Hilaly R. Diagnostic ultrasound of the vagus nerve in patients with diabetes. J Neuroimaging. 2017; 27: 589–93. DOI: 10.1111/jon.12452.
  16. Tsukita K, Taguchi T, Sakamaki-Tsukita H, Tanaka K, Suenaga T. Vagus nerve atrophy in Parkinson’s disease detected by ultrasonography. Journal of the Neurological Sciences. 2017; 365, 129. DOI: 10.1016/j.jns.2017.08.391.
  17. Tsukita K, Taguchi T, Sakamaki-Tsukita H, Tanaka K, Suenaga T. The vagus nerve becomes smaller in patients with Parkinson’s disease: a preliminary cross-sectional study using ultrasonography. Parkinsonism Relat Disord. 2018; 55: 148–49. DOI: 10.1016/j. parkreldis.2018.06.002.
  18. Fedtke N, Witte O, Prell T. Ultrasonography of the vagus nerve in Parkinson’s disease. Front Neurol. 2018; 9: 525. DOI: 10.3389/ fneur.2018.00525.
  19. Walter U, Tsiberidou P, Kersten M, Storch A, Lohle M. Atrophy of the vagus nerve in Parkinson’s Disease revealed by highresolution ultrasonography. Front Neurol. 2018; 9: 805. DOI: 10.3389/fneur.2018.00805.
  20. Pelz J, Belau E, Fricke C, Classen J, Weise D. Axonal degeneration of the vagus nerve in Parkinson’s disease-a high-resolution ultrasound study. Front Neurol. 2018; 9: 951. DOI: 10.3389/ fneur.2018.00951.
  21. Laucius O, Balnyte R, Petrikonis K, Matijosaitis V, Juceviciute N, Vanagas T, et al. Ultrasonography of the vagus nerve in the diagnosis of Parkinson’s disease. Parkinsons Dis. 2020; 2020: 2627471. DOI: 10.1155/2020/2627471.
  22. Sijben L, Mess W, Walter U, Janssen A, Kuijf M, Oosterloo M. The cross-sectional area of the vagus nerve is not reduced in Parkinson’s Disease patients. medRxiv [Preprint]. 2020. DOI: 10.1101/2020.10.19.20214973.
  23. Sartucci F, Bocci T, Santin M, Bongioanni P, Orlandi G. Highresolution ultrasound changes of the vagus nerve in idiopathic Parkinson’s disease (IPD): a possible additional index of disease. Neurol Sci. 2021. DOI: 10.1007/s10072-021-05183-5.
  24. Fedotova EYu, Chechetkin AO, Shadrina MI, Slominsky PA, Ivanova-Smolenskaya IA, Illarioshkin SN. Transcranial sonography in Parkinson’s disease. Zh Nevrol Psikhiatr Im SS Korsakova. 2011; 1: 49–55.
  25. Pelz J, Belau E, Henn P, Hammer N, Classen J, Weise D. Sonographic evaluation of the vagus nerves: protocol, reference values, and side-to-side differences. Muscle Nerve. 2018; 57 (5): 766–71. DOI: 10.1002/mus.25993.
  26. Verlinden T, Rijkers K, Hoogland G, Herrler A. Morphology of the human cervical vagus nerve: implications for vagus nerve stimulation treatment. Acta Neurol Scand. 2016; 133: 173–82. DOI: 10.1111/ane.12462.
  27. Hoffman H, Schnitzlein H. The numbers of nerve fibers in the vagus nerve of man. Anat Rec. 1961; 139: 429–35. DOI: 10.1002/ ar.1091390312.
  28. Cheng Z, Powley T, Schwaber J, Doyle F. Projections of the dorsal motor nucleus of the vagus to cardiac ganglia of rat atria: an anterograde tracing study. J Comp Neurol. 1999; 410: 320–41.
  29. Braak H, Del Tredici K, Rub U, de Vos R, Steur J, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003; 24: 197–211. DOI: 10.1016/S01974580(02)00065-9.
  30. Fedotova EYu, Chechetkin AO, Abramycheva NYu, Chigaleychik LA, Baziyan BKh, Ponomareva ТА, et al. Identification of people at the latent stage of Parkinson’s disease (the PARKINLAR study): first results and an optimization of the algorithm. Zh Nevrol Psikhiatr Im S S Korsakova. 2015; 115 (6): 4–11. DOI: 10.17116/ jnevro2015115614-11.