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Dysphagia in Parkinson Disease: Part II—Current Treatment Options and Insights from Animal Research

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Abstract

Purpose of Review

Dysphagia is highly prevalent in Parkinson disease (PD) but is not typically identified nor treated until later in the disease process. This review summarizes current pharmacological, surgical, and behavioral treatments for PD-associated dysphagia and contributions from translational animal research.

Recent Findings

Swallowing is a complex physiologic process controlled by multiple brain regions and neurotransmitter systems. As such, interventions that target nigrostriatal dopamine dysfunction have limited or detrimental effects on swallowing outcomes. Behavioral interventions can help target PD-associated dysphagia in mid-to-late stages. Animal research is necessary to refine treatments and useful in studying prodromal dysphagia.

Summary

Dysphagia is an early, common, and debilitating sign of PD. Current pharmacological and surgical interventions are not effective in ameliorating swallowing dysfunction; behavioral intervention remains the most effective approach for dysphagia treatment. Animal research has advanced our understanding of mechanisms underlying PD and PD-associated dysphagia, and continues to show translational promise for the study of dysphagia treatment options.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Schapira AHV, Chaudhuri KR, Jenner P. Non-motor features of Parkinson disease. Nat Rev Neurosci. 2017;18:435–50. https://doi.org/10.1038/nrn.2017.62.

    Article  CAS  PubMed  Google Scholar 

  2. Plowman-Prine EK, Sapienza CM, Okun MS, Pollock SL, Jacobson C, Wu SS, Rosenbek JC. The relationship between quality of life and swallowing in Parkinson’s disease. Mov Disord. 2009;24:1352–8. https://doi.org/10.1002/mds.22617.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Suttrup I, Warnecke T. Dysphagia in Parkinson’s disease. Dysphagia. 2016;31:24–32. https://doi.org/10.1007/s00455-015-9671-9.

    Article  PubMed  Google Scholar 

  4. Fernandez HH, Lapane KL. Predictors of mortality among nursing home residents with a diagnosis of Parkinson’s disease. Med Sci Monit. 2002;8:241–6.

    Google Scholar 

  5. Del Tredici K, Braak H. Dysfunction of the locus coeruleus-norepinephrine system and related circuitry in Parkinson’s disease-related dementia. J Neurol Neurosurg Psychiatry. 2013;84:774–83. https://doi.org/10.1136/jnnp-2011-301817.

    Article  PubMed  Google Scholar 

  6. Beattie DT, Smith JAM. Serotonin Pharmacology in the gastrointestinal tract: a review. Naunyn Schmiedebergs Arch Pharmacol. 2008;377:181–203. https://doi.org/10.1007/s00210-008-0276-9.

    Article  CAS  PubMed  Google Scholar 

  7. Marras C, Chaudhuri KR, Titova N, Mestre TA. Therapy of Parkinson’s disease subtypes. Neurotherapeutics. 2020;17(4):1366–77. https://doi.org/10.1007/S13311-020-00894-7.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Beach TG, Adler CH, Sue LI, Vedders L, Lue LF, White CL, Akiyama H, Caviness JN, Shill HA, Sabbagh MN, et al. Multi-organ distribution of phosphorylated α-synuclein histopathology in subjects with Lewy body disorders. Acta Neuropathol. 2010;119:689–702. https://doi.org/10.1007/s00401-010-0664-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wang E, Kompoliti K, Jiang JJ, Goetz CG. an instrumental analysis of laryngeal responses to apomorphine stimulation in Parkinson disease. J Med Speech Lang Pathol. 2000;8:175–86.

    Google Scholar 

  10. Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, Lang AE, Deuschl G. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord. 2006;21:S290–304. https://doi.org/10.1002/mds.20962.

    Article  PubMed  Google Scholar 

  11. Ossig C, Reichmann H. Treatment strategies in early and advanced Parkinson disease. Neurol Clin. 2015;33:19–37. https://doi.org/10.1016/j.ncl.2014.09.009.

    Article  PubMed  Google Scholar 

  12. Horstink M, Tolosa E, Bonuccelli U, Deuschl G, Friedman A, Kanovsky P, Larsen JP, Lees A, Oertel W, Poewe W, et al. Review of the therapeutic management of Parkinson’s disease. Report of a Joint Task Force of the European Federation of Neurological Societies and the Movement Disorder Society-European Section. Part I: Early (uncomplicated) Parkinson’s disease. Eur J Neurol. 2006;13:1170–85. https://doi.org/10.1111/j.1468-1331.2006.01547.x.

    Article  CAS  PubMed  Google Scholar 

  13. Fox SH, Katzenschlager R, Lim S-Y, Barton B, de Bie RMA, Seppi K, Coelho M, Sampaio C. International Parkinson and movement disorder society evidence-based medicine review: update on treatments for the motor symptoms of Parkinson’s disease. Mov Disord. 2018;33:1248–66. https://doi.org/10.1002/mds.27372.

    Article  CAS  PubMed  Google Scholar 

  14. Suttrup I, Warnecke T. Dysphagia in Parkinson’s disease: pathophysiology, diagnosis and therapy. Fortschritte der Neurologie Psychiatrie. 2016;84:S18–23. https://doi.org/10.1055/s-0042-107245.

    Article  PubMed  Google Scholar 

  15. Langmore SE. Evaluation of oropharyngeal dysphagia: which diagnostic tool is superior? Curr Opin Otolaryngol Head Neck Surg. 2003;11:485–9. https://doi.org/10.1097/00020840-200312000-00014.

    Article  PubMed  Google Scholar 

  16. Labeit B, Claus I, Muhle P, Suntrup-Krueger S, Dziewas R, Warnecke T. Effect of intestinal levodopa-carbidopa infusion on pharyngeal dysphagia: results from a retrospective pilot study in patients with Parkinson’s disease. Parkinsons Dis. 2020;2020:4260501. https://doi.org/10.1155/2020/4260501.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Warnecke T, Suttrup I, Schröder JB, Osada N, Oelenberg S, Hamacher C, Suntrup S, Dziewas R. Levodopa responsiveness of dysphagia in advanced Parkinson’s disease and reliability testing of the FEES-levodopa-test. Parkinsonism Relat Disord. 2016;28:100–6. https://doi.org/10.1016/j.parkreldis.2016.04.034.

    Article  PubMed  Google Scholar 

  18. Hacker ML, Turchan M, Heusinkveld LE, Currie AD, Millan SH, Molinari AL, Konrad PE, Davis TL, Phibbs FT, Hedera P, et al. Deep brain stimulation in early-stage Parkinson disease: five-year outcomes. Neurology. 2020;95:e393–401. https://doi.org/10.1212/WNL.0000000000009946.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ciucci MR, Barkmeier-Kraemer JM, Sherman SJ. Subthalamic nucleus deep brain stimulation improves deglutition in Parkinson’s disease. Mov Disord. 2008;23:676–83. https://doi.org/10.1002/mds.21891.

    Article  PubMed  Google Scholar 

  20. Troche MS, Okun MS, Rosenbek JC, Musson N, Fernandez HH, Rodriguez R, Romrell J, Pitts T, Wheeler-Hegland KM, Sapienza CM. Aspiration and swallowing in Parkinson disease and rehabilitation with EMST: a randomized trial. Neurology. 2010;75:1912–9. https://doi.org/10.1212/WNL.0b013e3181fef115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8. https://doi.org/10.1007/BF00417897.

    Article  CAS  PubMed  Google Scholar 

  22. Gandhi P, Steele CM. Effectiveness of interventions for dysphagia in Parkinson disease: a systematic review. Am J Speech Lang Pathol. 2022;31:463–85. https://doi.org/10.1044/2021_AJSLP-21-00145.

    Article  PubMed  Google Scholar 

  23. Pflug C, Nienstedt JC, Gulberti A, Müller F, Vettorazzi E, Koseki JC, Niessen A, Flügel T, Hidding U, Buhmann C, et al. Impact of simultaneous subthalamic and nigral stimulation on dysphagia in Parkinson’s disease. Ann Clin Transl Neurol. 2020;7:628–38. https://doi.org/10.1002/acn3.51027.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Khedr EM, Al-Fawal B, Abdel Wraith A, Saber M, Hasan AM, Bassiony A, Nasr Eldein A, Rothwell JC. The effect of 20 Hz versus 1 Hz repetitive transcranial magnetic stimulation on motor dysfunction in Parkinson’s disease: which is more beneficiaL? J Parkinsons Dis. 2019;9:379–87. https://doi.org/10.3233/JPD-181540.

    Article  PubMed  Google Scholar 

  25. Ra JY, Hyun JK, Ko KR, Lee SJ. Chin tuck for prevention of aspiration: effectiveness and appropriate posture. Dysphagia. 2014;29:603–9. https://doi.org/10.1007/s00455-014-9551-8.

    Article  PubMed  Google Scholar 

  26. Karvonen J, Saarelainen S, Nieminen MM. Measurement of respiratory muscle forces based on maximal inspiratory and expiratory pressures. Respiration. 1994;61:28–31. https://doi.org/10.1159/000196299.

    Article  CAS  PubMed  Google Scholar 

  27. Sapienza C, Troche M, Pitts T, Davenport P. Respiratory strength training: concept and intervention outcomes. Semin Speech Lang. 2011;32:21–30. https://doi.org/10.1055/s-0031-1271972.

    Article  PubMed  Google Scholar 

  28. van de Wetering-van Dongen VA, Kalf JG, van der Wees PJ, Bloem BR, Nijkrake MJ. The effects of respiratory training in Parkinson’s disease: a systematic review. J Parkinsons Dis. 2020;10:1315–33. https://doi.org/10.3233/jpd-202223.

    Article  PubMed  PubMed Central  Google Scholar 

  29. •• Troche MS, Curtis JA, Sevitz JS, Dakin AE, Perry SE, Borders JC, Grande AA, Mou Y, Vanegas-Arroyave N, Hegland KW. rehabilitating cough dysfunction in Parkinson’s disease: a randomized controlled trial. Mov Disord. 2022. https://doi.org/10.1002/mds.29268. Findings from this trial confirm the efficacy of behavioral interventions for cough-related outcomes in PD.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Reyes A, Castillo A, Castillo J, Cornejo I. The effects of respiratory muscle training on peak cough flow in patients with Parkinson’s disease: a randomized controlled study. Clin Rehabil. 2018;32:1317–27. https://doi.org/10.1177/0269215518774832.

    Article  PubMed  Google Scholar 

  31. Pitts T, Bolser D, Rosenbek J, Troche M, Okun MS, Sapienza C. Impact of expiratory muscle strength training on voluntary cough and swallow function in Parkinson disease. Chest. 2009;135:1301–8. https://doi.org/10.1378/chest.08-1389.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Reyes A, Castillo A, Castillo J. Effects of expiratory muscle training and air stacking on peak cough flow in individuals with Parkinson’s disease. Lung. 2020;198:207–11. https://doi.org/10.1007/s00408-019-00291-8.

    Article  PubMed  Google Scholar 

  33. Hutcheson KA, Hammer MJ, Rosen SP, Jones CA, McCulloch TM. Expiratory muscle strength training evaluated with simultaneous high-resolution manometry and electromyography. Laryngoscope. 2017;127:797–804. https://doi.org/10.1002/lary.26397.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Pauloski BR, Yahnke KM. Using ultrasound to document the effects of expiratory muscle strength training (EMST) on the geniohyoid muscle. Dysphagia. 2022;37:788–99. https://doi.org/10.1007/s00455-021-10328-x.

    Article  PubMed  Google Scholar 

  35. Inzelberg R, Peleg N, Nisipeanu P, Magadle R, Carasso RL, Weiner P. Inspiratory muscle training and the perception of dyspnea in Parkinson’s disease. Can J Neurol Sci. 2005;32:213–7. https://doi.org/10.1017/S0317167100003991.

    Article  PubMed  Google Scholar 

  36. Robertson SJ, Thomson F. Speech therapy in Parkinson’s disease: a study of the efficacy and long term effects of intensive treatment. Br J Disord Commun. 1984;19:213–24. https://doi.org/10.3109/13682828409029837.

    Article  CAS  PubMed  Google Scholar 

  37. el Sharkawi A, Ramig L, Logemann JA, Pauloski BR, Rademaker AW, Smith CH, Pawlas A, Baum S, Werner C. Swallowing and voice effects of Lee Silverman Voice Treatment (LSVT®): a pilot study. J Neurol Neurosurg Psychiatry. 2002;72:31–6. https://doi.org/10.1136/jnnp.72.1.31.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Miles A, Jardine M, Johnston F, de Lisle M, Friary P, Allen J. Effect of Lee Silverman Voice Treatment (LSVT LOUD®) on swallowing and cough in Parkinson’s disease: a pilot study. J Neurol Sci. 2017;383:180–7. https://doi.org/10.1016/j.jns.2017.11.015.

    Article  PubMed  Google Scholar 

  39. Quittan M, Wiesinger GF, Sturm B, Puig S, Mayr W, Sochor A, Paternostro T, Resch KL, Pacher R, Fialka-Moser V. Improvement of thigh muscles by neuromuscular electrical stimulation in patients with refractory heart failure: a single-blind, randomized, controlled trial. Am J Phys Med Rehabil. 2001;80:206–14. https://doi.org/10.1097/00002060-200103000-00011.

    Article  CAS  PubMed  Google Scholar 

  40. Park JS, Oh DH, Hwang NK, Lee JH. Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial. NeuroRehabilitation. 2018;42:457–63. https://doi.org/10.3233/NRE-172306.

    Article  PubMed  Google Scholar 

  41. Baijens LWJ, Speyer R, Passos VL, Pilz W, Van Der Kruis J, Haarmans S, Desjardins-Rombouts C. Surface electrical stimulation in dysphagic Parkinson patients: a randomized clinical trial. Laryngoscope. 2013;123:E38-44. https://doi.org/10.1002/lary.24119.

    Article  PubMed  Google Scholar 

  42. Jenks J, Pitts LL. Effects of an intensive exercise-based swallowing program for persons with Parkinson’s disease and complex medical history: a single-case experiment. Am J Speech Lang Pathol. 2019;28:1268–74. https://doi.org/10.1044/2019_AJSLP-18-0168.

    Article  PubMed  Google Scholar 

  43. Curtis JA, Dakin AE, Troche MS. Respiratory–swallow coordination training and voluntary cough skill training: a single-subject treatment study in a person with Parkinson’s disease. J Speech Lang Hear Res. 2020;63:472–86. https://doi.org/10.1044/2019_JSLHR-19-00207.

    Article  PubMed  Google Scholar 

  44. Bloem BR, de Vries NM, Ebersbach G. Nonpharmacological treatments for patients with Parkinson’s disease. Mov Disord. 2015;30:1504–20. https://doi.org/10.1002/mds.26363.

    Article  PubMed  Google Scholar 

  45. Manor Y, Mootanah R, Freud D, Giladi N, Cohen JT. Video-assisted swallowing therapy for patients with Parkinson’s disease. Parkinsonism Relat Disord. 2013;19:207–11. https://doi.org/10.1016/j.parkreldis.2012.10.004.

    Article  PubMed  Google Scholar 

  46. Sarmento A, de Andrade AFD, Lima ÍNDF, Aliverti A, de Freitas Fregonezi GA, Resqueti VR. Air stacking: a detailed look into physiological acute effects on cough peak flow and chest wall volumes of healthy subjects. Respir Care. 2017;62:432–43. https://doi.org/10.4187/respcare.05189.

    Article  PubMed  Google Scholar 

  47. Hegland KW, Okun MS, Troche MS. Sequential voluntary cough and aspiration or aspiration risk in Parkinson’s disease. Lung. 2014;192:601–8. https://doi.org/10.1007/s00408-014-9584-7.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Warnecke T, Hamacher C, Oelenberg S, Dziewas R. Off and on state assessment of swallowing function in Parkinson’s disease. Parkinsonism Relat Disord. 2014;20:1033–4. https://doi.org/10.1016/j.parkreldis.2014.06.016.

    Article  PubMed  Google Scholar 

  49. Rogus-Pulia NM, Plowman EK. Shifting tides toward a proactive patient-centered approach in dysphagia management of neurodegenerative disease. Am J Speech Lang Pathol. 2020;29:1094–109. https://doi.org/10.1044/2020_AJSLP-19-00136.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Barbe AG, Heinzler A, Derman S, Hellmich M, Timmermann L, Noack MJ. Hyposalivation and xerostomia among Parkinson’s disease patients and its impact on quality of life. Oral Dis. 2017;23:464–70. https://doi.org/10.1111/odi.12622.

    Article  CAS  PubMed  Google Scholar 

  51. Bagheri H, Damase-Michel C, Lapeyre-Mestre M, Cismondo S, O’Connell D, Senard JM, Rascol O, Montastruc JL. A study of salivary secretion in Parkinson’s disease. Clin Neuropharmacol. 1999;22:213–5.

    CAS  PubMed  Google Scholar 

  52. Kalf JG, De Swart BJM, Borm GF, Bloem BR, Munneke M. Prevalence and definition of drooling in Parkinson’s disease: a systematic review. J Neurol. 2009;256:1391–6. https://doi.org/10.1007/s00415-009-5098-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Bird AM, Smith TL, Walton AE. Un Repaso de Las Estrategias de Tratamiento Actuales de La Sialorrea Inducida Por Clozapina. Ann Pharmacother. 2011;45:667–75. https://doi.org/10.1345/aph.1P761.

    Article  CAS  PubMed  Google Scholar 

  54. Tumilasci OR, Cersósimo MG, Belforte JE, Micheli FE, Benarroch EE, Pazo JH. Quantitative study of salivary secretion in Parkinson’s disease. Mov Disord. 2006;21:660–7. https://doi.org/10.1002/mds.20784.

    Article  PubMed  Google Scholar 

  55. Arany S, Kopycka-Kedzierawski DT, Caprio TV, Watson GE. Anticholinergic medication: related dry mouth and effects on the salivary glands. Oral Surg Oral Med Oral Pathol Oral Radiol. 2021;132:662–70. https://doi.org/10.1016/j.oooo.2021.08.015.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Isaacson J, Patel S, Torres-Yaghi Y, Pagán F. Sialorrhea in Parkinson’s disease. Toxins (Basel). 2020;12:691. https://doi.org/10.3390/toxins12110691.

    Article  CAS  PubMed  Google Scholar 

  57. Łysik D, Niemirowicz-Laskowska K, Bucki R, Tokajuk G, Mystkowska J. Artificial saliva: challenges and future perspectives for the treatment of xerostomia. Int J Mol Sci. 2019;20:3199. https://doi.org/10.3390/ijms20133199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gil-Montoya JA, Silvestre FJ, Barrios R, Silvestre-Rangil J. Treatment of xerostomia and hyposalivation in the elderly: a systematic review. Med Oral Patol Oral Cir Bucal. 2016;21:e355–66. https://doi.org/10.4317/medoral.20969.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Srivanitchapoom P, Pandey S, Hallett M. Drooling in Parkinson’s disease: a review. Parkinsonism Relat Disord. 2014;20:1109–18. https://doi.org/10.1016/j.parkreldis.2014.08.013.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Marks L, Turner K, O’Sullivan J, Deighton B, Lees A. Drooling in Parkinson’s disease: a novel speech and language therapy intervention. Int J Lang Commun Disord. 2001;36:282–7. https://doi.org/10.3109/13682820109177898.

    Article  PubMed  Google Scholar 

  61. Postma AG, Heesters MAAM, van Laar T. Radiotherapy to the salivary glands as treatment of sialorrhea in patients with parkinsonism. Mov Disord. 2007;22:2430–5. https://doi.org/10.1002/mds.21752.

    Article  PubMed  Google Scholar 

  62. South AR, Somers SM, Jog MS. Gum chewing improves swallow frequency and latency in Parkinson patients: a preliminary study. Neurology. 2010;74:1198–202. https://doi.org/10.1212/WNL.0b013e3181d9002b.

    Article  PubMed  Google Scholar 

  63. Potts LF, Wu H, Singh A, Marcilla I, Luquin MR, Papa SM. Modeling Parkinson’s disease in monkeys for translational studies, a critical analysis. Exp Neurol. 2014;256:133–43. https://doi.org/10.1016/j.expneurol.2013.09.014.

    Article  CAS  PubMed  Google Scholar 

  64. Tieu K. A guide to neurotoxic animal models of Parkinson’s disease. Cold Spring Harb Perspect Med. 2011;1:a009316–a009316. https://doi.org/10.1101/cshperspect.a009316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Plowman EK, Maling N, Thomas NJ, Fowler SC, Kleim JA. targeted motor rehabilitation dissociates corticobulbar versus corticospinal dysfunction in an animal model of Parkinson’s disease. Neurorehabil Neural Repair. 2014;28:85–95. https://doi.org/10.1177/1545968313498648.

    Article  PubMed  Google Scholar 

  66. Ciucci MR, Russell JA, Schaser AJ, Doll EJ, Vinney LM, Connor NP. Tongue force and timing deficits in a rat model of Parkinson disease. Behav Brain Res. 2011;222:315–20. https://doi.org/10.1016/j.bbr.2011.03.057.

    Article  PubMed  Google Scholar 

  67. Kane JR, Ciucci MR, Jacobs AN, Tews N, Russell JA, Ahrens AM, Ma ST, Britt JM, Cormack LK, Schallert T. Assessing the role of dopamine in limb and cranial-oromotor control in a rat model of Parkinson’s disease. J Commun Disord. 2011;44:529–37. https://doi.org/10.1016/j.jcomdis.2011.04.005.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Russell JA, Ciucci MR, Hammer MJ, Connor NP. Videofluorographic assessment of deglutitive behaviors in a rat model of aging and Parkinson disease. Dysphagia. 2013;28:95–104. https://doi.org/10.1007/s00455-012-9417-x.

    Article  PubMed  Google Scholar 

  69. Tillerson JL, Caudle WM, Reverón ME, Miller GW. Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson’s disease. Neuroscience. 2003;119:899–911. https://doi.org/10.1016/S0306-4522(03)00096-4.

    Article  CAS  PubMed  Google Scholar 

  70. Waters CM, Hunt SP, Jenner P, Marsden CD. An immunohistochemical study of the acute and long-term effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in the marmoset. Neuroscience. 1987;23:1025–39. https://doi.org/10.1016/0306-4522(87)90178-3.

    Article  CAS  PubMed  Google Scholar 

  71. Mikkelsen M, MØller A, Jensen LH, Pedersen A, Harajehi JB, Pakkenberg H. MPTP-induced parkinsonism in minipigs: a behavioral, biochemical, and histological study. Neurotoxicol Teratol. 1999;21:169–75. https://doi.org/10.1016/S0892-0362(98)00037-3.

    Article  CAS  PubMed  Google Scholar 

  72. Anstrom KK, Schallert T, Woodlee MT, Shattuck A, Roberts DCS. Repetitive vibrissae-elicited forelimb placing before and immediately after unilateral 6-hydroxydopamine improves outcome in a model of Parkinson’s disease. Behav Brain Res. 2007;179:183–91. https://doi.org/10.1016/j.bbr.2007.01.028.

    Article  CAS  PubMed  Google Scholar 

  73. Cohen AD, Tillerson JL, Smith AD, Schallert T, Zigmond MJ. Neuroprotective effects of prior limb use in 6-hydroxydopamine-treated rats: possible role of GDNF. J Neurochem. 2003;85:299–305. https://doi.org/10.1046/j.1471-4159.2003.01657.x.

    Article  CAS  PubMed  Google Scholar 

  74. Tillerson JL, Cohen AD, Philhower J, Miller GW, Zigmond MJ, Schallert T. Forced limb-use effects on the behavioral and neurochemical effects of 6-hydroxydopamine. J Neurosci. 2001;21:4427–35. https://doi.org/10.1523/jneurosci.21-12-04427.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Ciucci MR, Schaser AJ, Russell JA. Exercise-induced rescue of tongue function without striatal dopamine sparing in a rat neurotoxin model of Parkinson disease. Behav Brain Res. 2013;252:239–45. https://doi.org/10.1016/j.bbr.2013.06.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Deng H, Wang P, Jankovic J. The genetics of Parkinson disease. Ageing Res Rev. 2018;42:72–85. https://doi.org/10.1016/j.arr.2017.12.007.

    Article  CAS  PubMed  Google Scholar 

  77. Krasko MN, Hoffmeister JD, Schaen-Heacock NE, Welsch JM, Kelm-Nelson CA, Ciucci MR. Rat models of vocal deficits in Parkinson’s disease. Brain Sci. 2021;11:925. https://doi.org/10.3390/BRAINSCI11070925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Yang KM, Blue KV, Mulholland HM, Kurup MP, Kelm-Nelson CA, Ciucci MR. Characterization of oromotor and limb motor dysfunction in the DJ1 -/- model of Parkinson disease. Behav Brain Res. 2018;339:47–56. https://doi.org/10.1016/j.bbr.2017.10.036.

    Article  PubMed  Google Scholar 

  79. • Paredes-Rodriguez E, Vegas-Suarez S, Morera-Herreras T, de Deurwaerdere P, Miguelez C. The noradrenergic system in Parkinson’s disease. Front Pharmacol. 2020;11:435. https://doi.org/10.3389/fphar.2020.00435. This article demonstrates that other neurotransmitter systems beyond dopamine are implicated during the PD disease process. Specifically, it highlights the role of noradrenaline in PD.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Hoffmeister JD, Kelm-Nelson CA, Ciucci MR. Quantification of brainstem norepinephrine relative to vocal impairment and anxiety in the Pink1-/- rat model of Parkinson disease. Behav Brain Res. 2021;414:113514. https://doi.org/10.1016/j.bbr.2021.113514.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Dave KD, De Silva S, Sheth NP, Ramboz S, Beck MJ, Quang C, Switzer RC 3rd, Ahmad SO, Sunkin SM, Walker D, et al. Phenotypic characterization of recessive gene knockout rat models of Parkinson’s disease. Neurobiol Dis 2014;70:190–203https://doi.org/10.1016/j.nbd.2014.06.009

  82. Cullen KP, Grant LM, Kelm-Nelson CA, Brauer AFL, Bickelhaupt LB, Russell JA, Ciucci MR. Pink1 -/- rats show early-onset swallowing deficits and correlative brainstem pathology. Dysphagia. 2018;33:749–58. https://doi.org/10.1007/s00455-018-9896-5.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Marquis JM, Lettenberger SE, Kelm-Nelson CA. Early-onset Parkinsonian behaviors in female Pink1-/- rats. Behav Brain Res. 2020;377:112175. https://doi.org/10.1016/j.bbr.2019.112175.

    Article  CAS  PubMed  Google Scholar 

  84. Grant LM, Kelm-Nelson CA, Hilby BL, Blue KV, Paul Rajamanickam ES, Pultorak JD, Fleming SM, Ciucci MR. Evidence for early and progressive ultrasonic vocalization and oromotor deficits in a PINK1 gene knockout rat model of Parkinson’s disease. J Neurosci Res. 2015;93:1713–27. https://doi.org/10.1002/jnr.23625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Krasko, M. N., Szot, J., Lungova, K., Rowe, L. M., Leverson, G., Kelm-Nelson, C. A., & Ciucci, M. R. (2023). Pink1-/-Rats Demonstrate Swallowing and Gastrointestinal Dysfunction in a Model of Prodromal Parkinson Disease. Dysphagia, 1–16.

  86. Glass TJ, Kelm-Nelson CA, Szot JC, Lake JM, Connor NP, Ciucci MR. Functional characterization of extrinsic tongue muscles in the Pink1-/- rat model of Parkinson disease. PLoS ONE. 2020;15:e0240366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Connor NP, Russell JA, Wang H, Jackson MA, Mann L, Kluender K. Effect of tongue exercise on protrusive force and muscle fiber area in aging rats. J Speech Lang Hear Res. 2009;52:732–44. https://doi.org/10.1044/1092-4388(2008/08-0105).

    Article  PubMed  Google Scholar 

  88. Rudisch DM, Krasko MN, Nisbet AF, Schaen-Heacock NE, Ciucci MR. Assays of tongue force, timing, and dynamics in rat and mouse models. Brain Res Bull. 2022;185:49–55. https://doi.org/10.1016/j.brainresbull.2022.04.008.

    Article  PubMed  Google Scholar 

  89. Schaser AJ, Ciucci MR, Connor NP. Cross-activation and detraining effects of tongue exercise in aged rats. Behav Brain Res. 2016;297:285–96. https://doi.org/10.1016/j.bbr.2015.10.030.

    Article  PubMed  Google Scholar 

  90. Schaser AJ, Stang K, Connor NP, Behan M. The effect of age and tongue exercise on BDNF and TrkB in the hypoglossal nucleus of rats. Behav Brain Res. 2012;226:235–41. https://doi.org/10.1016/j.bbr.2011.09.027.

    Article  CAS  PubMed  Google Scholar 

  91. Krekeler BN, Weycker JM, Connor NP. Effects of tongue exercise frequency on tongue muscle biology and swallowing physiology in a rat model. Dysphagia. 2020;35:918–34. https://doi.org/10.1007/s00455-020-10105-2.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Cunningham DP, Basmajian JV. Electromyography of genioglossus and geniohyoid muscles during deglutition. Anat Rec. 1969;165:401–9. https://doi.org/10.1002/ar.1091650309.

    Article  CAS  PubMed  Google Scholar 

  93. Bole CT, Lessler MA. Electromyography of the genioglossus muscles in man. J Appl Physiol. 1966;21:1695–8. https://doi.org/10.1152/JAPPL.1966.21.6.1695.

    Article  PubMed  Google Scholar 

  94. Mathew OP, Abu-Osba YK, Thach BT. Influence of upper airway pressure changes on genioglossus muscle respiratory activity. J Appl Physiol Respir Environ Exerc Physiol. 1982;52:438–44. https://doi.org/10.1152/jappl.1982.52.2.438.

    Article  CAS  PubMed  Google Scholar 

  95. Behan M, Moeser AE, Thomas CF, Russell JA, Wang H, Leverson GE, Connor NP. The effect of tongue exercise on serotonergic input to the hypoglossal nucleus in young and old rats. J Speech Lang Hear Res. 2012;55:919–29. https://doi.org/10.1044/1092-4388(2011/11-0091).

    Article  PubMed  Google Scholar 

  96. Broadfoot CK, Abur D, Hoffmeister JD, Stepp CE, Ciucci MR. Research-based updates in swallowing and communication dysfunction in Parkinson disease: implications for evaluation and management. Perspect ASHA Spec Interest Groups. 2019;4:825–41. https://doi.org/10.1044/2019_PERS-SIG3-2019-0001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Miller N, Allcock L, Hildreth AJ, Jones D, Noble E, Burn DJ. Swallowing problems in Parkinson disease: frequency and clinical correlates. J Neurol Neurosurg Psychiatry. 2009;80:1047–9. https://doi.org/10.1136/jnnp.2008.157701.

    Article  CAS  PubMed  Google Scholar 

  98. Kalf JG, de Swart BJM, Bloem BR, Munneke M. Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Parkinsonism Relat Disord. 2012;18:311–5. https://doi.org/10.1016/j.parkreldis.2011.11.006.

    Article  CAS  PubMed  Google Scholar 

  99. Tolosa E, Garrido A, Scholz SW, Poewe W. Challenges in the diagnosis of Parkinson’s disease. Lancet Neurol. 2021;20:385–97. https://doi.org/10.1016/S1474-4422(21)00030-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Armstrong MJ, Okun MS. Diagnosis and treatment of Parkinson disease: a review. JAMA. 2020;323:548–60. https://doi.org/10.1001/JAMA.2019.22360.

    Article  PubMed  Google Scholar 

  101. National Institutes of Health. NIH guidelines on the inclusion of women and minorities as subjects in clinical research. Fed Regist. 1994;1994(59):1408–13.

    Google Scholar 

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Funding

This work was supported by the National Institute on Deafness and Other Communication Disorders of the National Institutes of Health (T32DC009401, appointee: Krasko; R01 DC018584, Ciucci; R01 DC014358, Ciucci), the National Institute on Aging of the National Institutes of Health (1K76AG068590, Rogus-Pulia), the University of Wisconsin-Madison, and the William S. Middleton Veteran Affairs Hospital in Madison, WI; GRECC article no. 2023-XXX.

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Authors and Affiliations

  1. Department of Surgery, Division of Otolaryngology—Head and Neck Surgery, University of Wisconsin-Madison, 1300 University Ave, Madison, WI, 53706, USA

    Maryann N. Krasko, Denis Michael Rudisch & Michelle R. Ciucci

  2. Department of Communication Sciences and Disorders, University of Wisconsin-Madison, 1975 Willow Drive, Madison, WI, 53706, USA

    Maryann N. Krasko, Denis Michael Rudisch & Michelle R. Ciucci

  3. Department of Medicine, Division of Geriatrics and Gerontology, School of Medicine and Public Health, University of Wisconsin-Madison, 1685 Highland Avenue, Madison, WI, 53705, USA

    Ryan J. Burdick, Nicole E. Schaen-Heacock, Courtney K. Broadfoot & Nicole Rogus-Pulia

  4. Geriatric Research Education and Clinical Center, William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, Madison, WI, 53705, USA

    Ryan J. Burdick, Nicole E. Schaen-Heacock, Courtney K. Broadfoot & Nicole Rogus-Pulia

  5. Perelman School of Medicine, University of Pennsylvania, 3400 Civic Center Blvd, Philadelphia, PA, 19104, USA

    Alex F. Nisbet

  6. Neuroscience Training Program, University of Wisconsin-Madison, 1111 Highland Ave, Madison, WI, 53705, USA

    Michelle R. Ciucci

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  1. Maryann N. Krasko
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Correspondence to Maryann N. Krasko.

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Dr. Michelle R. Ciucci is on the board of directors of the National Foundation of Swallowing Disorders (NFOSD) and receives no compensation as member of the board of directors.

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Maryann N. Krasko and Denis Michael Rudisch are co-first authors

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Krasko, M.N., Rudisch, D.M., Burdick, R.J. et al. Dysphagia in Parkinson Disease: Part II—Current Treatment Options and Insights from Animal Research. Curr Phys Med Rehabil Rep 11, 188–198 (2023). https://doi.org/10.1007/s40141-023-00393-8

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