Advertisement

Journal of Neural Transmission

, Volume 122, Issue 11, pp 1553–1561 | Cite as

Central cholinergic dysfunction could be associated with oropharyngeal dysphagia in early Parkinson’s disease

  • Kyung Duck Lee
  • Jung Hoi Koo
  • Sun Hong Song
  • Kwang Deog Jo
  • Moon Kyu Lee
  • Wooyoung JangEmail author
Neurology and Preclinical Neurological Studies - Original Article

Abstract

Dysphagia is an important issue in the prognosis of Parkinson’s disease (PD). Although several studies have reported that oropharyngeal dysphagia may be associated with cognitive dysfunction, the exact relationship between cortical function and swallowing function in PD patients is unclear. Therefore, we investigated the association between an electrophysiological marker of central cholinergic function, which reflected cognitive function, and swallowing function, as measured by videofluoroscopic studies (VFSS). We enrolled 29 early PD patients. Using the Swallowing Disturbance Questionnaire (SDQ), we divided the enrolled patients into two groups: PD with dysphagia and PD without dysphagia. The videofluoroscopic dysphagia scale (VDS) was applied to explore the nature of the dysphagia. To assess central cholinergic dysfunction, short latency afferent inhibition (SAI) was evaluated. We analyzed the relationship between central cholinergic dysfunction and oropharyngeal dysphagia and investigated the characteristics of the dysphagia. The SAI values were significantly different between the two groups. The comparison of each VFSS component between the PD with dysphagia group and the PD without dysphagia group showed statistical significance for most of the oral phase components and for a single pharyngeal phase component. The total score on the VDS was higher in the PD with dysphagia group than in the PD without dysphagia group. The Mini-Mental State Examination and SAI values showed significant correlations with the total score of the oral phase components. According to binary logistic regression analysis, SAI value independently contributed to the presence of dysphagia in PD patients. Our findings suggest that cholinergic dysfunction is associated with dysphagia in early PD and that an abnormal SAI value is a good biomarker for predicting the risk of dysphagia in PD patients.

Keywords

Parkinson’s disease Dysphagia Electrophysiology VFSS Short latency afferent inhibition 

Notes

Acknowledgments

This work was funded by the Gangneung Asan Hospital Biomedical Research Center Promotion Fund.

Compliance with ethical standards

Conflict of interest

The authors have reported no potential conflicts of interest concerning this article and have equally contributed to this study in a meaningful manner. None of the authors have anything to disclose.

References

  1. Bushmann M, Dobmeyer SM, Leeker L, Perlmutter JS (1989) Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology 39(10):1309CrossRefPubMedGoogle Scholar
  2. Celebi O, Temucin CM, Elibol B, Saka E (2012) Short latency afferent inhibition in Parkinson’s disease patients with dementia. Mov Disord 27(8):1052–1055CrossRefPubMedGoogle Scholar
  3. Cereda E, Cilia R, Klersy C, Canesi M, Zecchinelli AL, Mariani CB, Tesei S, Sacilotto G, Meucci N, Zini M, Isaias IU, Cassani E, Goldwurm S, Barichella M, Pezzoli G (2014) Swallowing disturbances in Parkinson’s disease: a multivariate analysis of contributing factors. Parkinsonism Relat Disord 20(12):1382–1387CrossRefPubMedGoogle Scholar
  4. Cersosimo MG, Benarroch EE (2012) Pathological correlates of gastrointestinal dysfunction in Parkinson’s disease. Neurobiol Dis 46(3):559–564CrossRefPubMedGoogle Scholar
  5. Chun SW, Lee SA, Jung IY, Beom J, Han TR, Oh BM (2011) Inter-rater agreement for the Clinical Dysphagia Scale. Ann Rehabil Med 35(4):470–476PubMedCentralCrossRefPubMedGoogle Scholar
  6. Di Lazzaro V, Oliviero A, Tonali PA, Marra C, Daniele A, Profice P, Saturno E, Pilato F, Masullo C, Rothwell JC (2002) Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology 59(3):392–397CrossRefPubMedGoogle Scholar
  7. Di Lazzaro V, Oliviero A, Saturno E, Dileone M, Pilato F, Nardone R, Ranieri F, Musumeci G, Fiorilla T, Tonali P (2005a) Effects of lorazepam on short latency afferent inhibition and short latency intracortical inhibition in humans. J Physiol 564(2):661–668PubMedCentralCrossRefPubMedGoogle Scholar
  8. Di Lazzaro V, Pilato F, Dileone M, Tonali PA, Ziemann U (2005b) Dissociated effects of diazepam and lorazepam on short-latency afferent inhibition. J Physiol 569(1):315–323PubMedCentralCrossRefPubMedGoogle Scholar
  9. Ertekin C (2014) Electrophysiological evaluation of oropharyngeal Dysphagia in Parkinson’s disease. J Mov Disord 7(2):31–56PubMedCentralCrossRefPubMedGoogle Scholar
  10. Evatt ML, Chaudhuri KR, Chou KL, Cubo E, Hinson V, Kompoliti K, Yang C, Poewe W, Rascol O, Sampaio C, Stebbins GT, Goetz CG (2009) Dysautonomia rating scales in Parkinson’s disease: sialorrhea, dysphagia, and constipation–critique and recommendations by movement disorders task force on rating scales for Parkinson’s disease. Mov Disord 24(5):635–646PubMedCentralCrossRefPubMedGoogle Scholar
  11. Fuh J-L, Lee R-C, Wang S-J, Lin C-H, Wang P-N, Chiang J-H, Liu H-C (1997) Swallowing difficulty in Parkinson’s disease. Clin Neurol Neurosurg 99(2):106–112CrossRefPubMedGoogle Scholar
  12. Grinberg LT, Rueb U, Alho AT, Heinsen H (2010) Brainstem pathology and non-motor symptoms in PD. J Neurol Sci 289(1–2):81–88CrossRefPubMedGoogle Scholar
  13. Han M, Ohnishi H, Nonaka M, Yamauchi R, Hozuki T, Hayashi T, Saitoh M, Hisahara S, Imai T, Shimohama S, Mori M (2011) Relationship between dysphagia and depressive states in patients with Parkinson’s disease. Parkinsonism Relat Disord 17(6):437–439CrossRefPubMedGoogle Scholar
  14. Hirano M, Isono C, Sakamoto H, Ueno S, Kusunoki S, Nakamura Y (2015) Rotigotine transdermal patch improves swallowing in dysphagic patients with Parkinson’s disease. Dysphagia 30(4):452–456CrossRefPubMedGoogle Scholar
  15. Hunter PC, Crameri J, Austin S, Woodward MC, Hughes AJ (1997) Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry 63(5):579–583PubMedCentralCrossRefPubMedGoogle Scholar
  16. Johnston BT, Li Q, Castell JA, Castell DO (1995) Swallowing and esophageal function in Parkinson’s disease. Am J Gastroenterol 90(10):1741–1746PubMedGoogle Scholar
  17. Kalf JG, Borm GF, de Swart BJ, Bloem BR, Zwarts MJ, Munneke M (2011) Reproducibility and validity of patient-rated assessment of speech, swallowing, and saliva control in Parkinson’s disease. Arch Phys Med Rehabil 92(7):1152–1158CrossRefPubMedGoogle Scholar
  18. Kalf JG, de Swart BJ, Bloem BR, Munneke M (2012) Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Parkinsonism Relat Disord 18(4):311–315CrossRefPubMedGoogle Scholar
  19. Kim DH, Choi KH, Kim HM, Koo JH, Kim BR, Kim TW, Ryu JS, Im S, Choi IS, Pyun SB, Park JW, Kang JY, Yang HS (2012) Inter-rater reliability of Videofluoroscopic Dysphagia Scale. Ann Rehabil Med 36(6):791–796PubMedCentralCrossRefPubMedGoogle Scholar
  20. Leopold NA, Kagel MC (1996) Prepharyngeal dysphagia in Parkinson’s disease. Dysphagia 11(1):14–22CrossRefPubMedGoogle Scholar
  21. Leopold NA, Kagel MC (1997) Pharyngo-esophageal dysphagia in Parkinson’s disease. Dysphagia 12(1):11–18CrossRefPubMedGoogle Scholar
  22. Luchesi KF, Kitamura S, Mourão LF (2013) Management of dysphagia in Parkinson’s disease and amyotrophic lateral sclerosis. In: CoDAS, vol 4, SciELO Brasil, pp 358–364Google Scholar
  23. Luchesi KF, Kitamura S, Mourao LF (2015) Dysphagia progression and swallowing management in Parkinson’s disease: an observational study. Braz J Otorhinolaryngol 81(1):24–30CrossRefPubMedGoogle Scholar
  24. Mancopes R, Busanello-Stella AR, Finger LS, Neu AP, Pacheco AdB, Torriani MS (2013) Influence of levodopa on the oral phase of swallowing in patients with Parkinson’s disease. Revista CEFAC 15(3):707–712CrossRefGoogle Scholar
  25. Manganelli F, Vitale C, Santangelo G, Pisciotta C, Iodice R, Cozzolino A, Dubbioso R, Picillo M, Barone P, Santoro L (2009) Functional involvement of central cholinergic circuits and visual hallucinations in Parkinson’s disease. Brain 132(Pt 9):2350–2355PubMedCentralCrossRefPubMedGoogle Scholar
  26. Manor Y, Giladi N, Cohen A, Fliss DM, Cohen JT (2007) Validation of a swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinson’s disease. Mov Disord 22(13):1917–1921CrossRefPubMedGoogle Scholar
  27. Martorana A, Mori F, Esposito Z, Kusayanagi H, Monteleone F, Codeca C, Sancesario G, Bernardi G, Koch G (2009) Dopamine modulates cholinergic cortical excitability in Alzheimer’s disease patients. Neuropsychopharmacology 34(10):2323–2328CrossRefPubMedGoogle Scholar
  28. Martorana A, Di Lorenzo F, Esposito Z, Lo Giudice T, Bernardi G, Caltagirone C, Koch G (2013) Dopamine D2-agonist Rotigotine effects on cortical excitability and central cholinergic transmission in Alzheimer’s disease patients. Neuropharmacology 64:108–113CrossRefPubMedGoogle Scholar
  29. Miller N, Noble E, Jones D, Burn D (2006) Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing 35(6):614–618CrossRefPubMedGoogle Scholar
  30. Monte FS, da Silva-Junior FP, Braga-Neto P, Nobre e Souza MA, de Bruin VM (2005) Swallowing abnormalities and dyskinesia in Parkinson’s disease. Mov Disord 20(4):457–462CrossRefPubMedGoogle Scholar
  31. Mu L, Sobotka S, Chen J, Su H, Sanders I, Nyirenda T, Adler CH, Shill HA, Caviness JN, Samanta JE, Sue LI, Beach TG (2013) Parkinson disease affects peripheral sensory nerves in the pharynx. J Neuropathol Exp Neurol 72(7):614–623PubMedCentralCrossRefPubMedGoogle Scholar
  32. Nagaya M, Kachi T, Yamada T, Igata A (1998) Videofluorographic study of swallowing in Parkinson’s disease. Dysphagia 13(2):95–100CrossRefPubMedGoogle Scholar
  33. Nagaya M, Kachi T, Yamada T, Sumi Y (2004) Videofluorographic observations on swallowing in patients with dysphagia due to neurodegenerative diseases. Nagoya J Med Sci 67(1–2):17–23PubMedGoogle Scholar
  34. Nardone R, Bratti A, Tezzon F (2006) Motor cortex inhibitory circuits in dementia with Lewy bodies and in Alzheimer’s disease. J Neural Transm 113(11):1679–1684CrossRefPubMedGoogle Scholar
  35. Nardone R, Bergmann J, Kronbichler M, Kunz A, Klein S, Caleri F, Tezzon F, Ladurner G, Golaszewski S (2008) Abnormal short latency afferent inhibition in early Alzheimer’s disease: a transcranial magnetic demonstration. J Neural Transm 115(11):1557–1562CrossRefPubMedGoogle Scholar
  36. Nardone R, Bergmann J, Christova M, Caleri F, Tezzon F, Ladurner G, Trinka E, Golaszewski S (2012) Short latency afferent inhibition differs among the subtypes of mild cognitive impairment. J Neural Transm (Vienna, Austria: 1996) 119(4):463–471CrossRefGoogle Scholar
  37. Nilsson H, Ekberg O, Olsson R, Hindfelt B (1996) Quantitative assessment of oral and pharyngeal function in Parkinson’s disease. Dysphagia 11(2):144–150CrossRefPubMedGoogle Scholar
  38. Potulska A, Friedman A, Królicki L, Spychala A (2003) Swallowing disorders in Parkinson’s disease. Parkinsonism Relat Disord 9(6):349–353CrossRefPubMedGoogle Scholar
  39. Robbins JA, Logemann JA, Kirshner HS (1986) Swallowing and speech production in Parkinson’s disease. Ann Neurol 19(3):283–287CrossRefPubMedGoogle Scholar
  40. Rofes L, Clave P, Ouyang A, Scharitzer M, Pokieser P, Vilardell N, Ortega O (2013) Neurogenic [corrected] and oropharyngeal dysphagia. Ann N Y Acad Sci 1300:1–10CrossRefPubMedGoogle Scholar
  41. Rolinski M, Fox C, Maidment I, McShane R (2012) Cholinesterase inhibitors for dementia with Lewy bodies, Parkinson's disease dementia and cognitive impairment in Parkinson's disease. Cochrane Database Syst Rev 3:Cd006504. doi: 10.1002/14651858.CD006504.pub2 PubMedGoogle Scholar
  42. Steele CM, Miller AJ (2010) Sensory input pathways and mechanisms in swallowing: a review. Dysphagia 25(4):323–333PubMedCentralCrossRefPubMedGoogle Scholar
  43. Suntrup S, Teismann I, Bejer J, Suttrup I, Winkels M, Mehler D, Pantev C, Dziewas R, Warnecke T (2013) Evidence for adaptive cortical changes in swallowing in Parkinson’s disease. Brain 136(Pt 3):726–738CrossRefPubMedGoogle Scholar
  44. Tjaden K (2008) Speech and swallowing in Parkinson’s disease. Top Geriatr Rehabil 24(2):115–126PubMedCentralCrossRefPubMedGoogle Scholar
  45. Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P, Rothwell JC (2000) Short latency inhibition of human hand motor cortex by somatosensory input from the hand. J Physiol 523(Pt 2):503–513PubMedCentralCrossRefPubMedGoogle Scholar
  46. Walshe M (2014) Oropharyngeal Dysphagia in Neurodegenerative Disease. J Gastroenterol Hepatol Res 3(10):1265–1271Google Scholar
  47. Yarnall AJ, Rochester L, Baker MR, David R, Khoo TK, Duncan GW, Galna B, Burn DJ (2013) Short latency afferent inhibition: a biomarker for mild cognitive impairment in Parkinson’s disease? Mov Disord 28(9):1285–1288CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Kyung Duck Lee
    • 1
  • Jung Hoi Koo
    • 1
  • Sun Hong Song
    • 1
  • Kwang Deog Jo
    • 2
  • Moon Kyu Lee
    • 2
  • Wooyoung Jang
    • 2
    • 3
    Email author
  1. 1.Department of Rehabilitation MedicineGangneung Asan Hospital, University of Ulsan College of MedicineGangneungRepublic of Korea
  2. 2.Department of NeurologyGangneung Asan Hospital, University of Ulsan College of MedicineGangneungRepublic of Korea
  3. 3.Biomedical Research CenterGangneung Asan HospitalGangneungRepublic of Korea

Personalised recommendations