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Impacts of Deep Brain Stimulation of the Globus Pallidus Internus on Swallowing: A Retrospective, Cross-Sectional Study

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Abstract

Deep brain stimulation (DBS) is a common treatment for motor symptoms of Parkinson disease (PD), a condition associated with increased risk of dysphagia. The effect of DBS on swallowing function has not been comprehensively evaluated using gold-standard imaging techniques, particularly for globus pallidus internus (GPi) DBS. The objective of this retrospective, cross-sectional study was to identify differences in swallowing safety and timing kinematics among PD subjects with and without GPi DBS. We investigated the effects of unilateral and bilateral GPi DBS as well as the relationship between swallowing safety and DBS stimulation parameters, using retrospective analysis of videofluoroscopy recordings (71 recordings from 36 subjects) from electronic medical records. Outcomes were analyzed by surgical status (pre-surgical, unilateral DBS, bilateral DBS). The primary outcome was percent of thin-liquid bolus trials rated as unsafe, with Penetration-Aspiration Scale scores of 3 or higher. Secondary analyses included swallowing timing measures, relationships between swallowing safety and DBS stimulation parameters, and Dynamic Imaging Grade of Swallowing Toxicity ratings. Most subjects swallowed all boluses safely (19/29 in the pre-surgical, 16/26 in the unilateral DBS, and 10/16 in the bilateral DBS conditions). Swallowing safety impairment did not differ among stimulation groups. There was no main effect of stimulation condition on timing metrics, though main effects were found for sex and bolus type. Stimulation parameters were not correlated with swallowing safety. Swallowing efficiency and overall impairment did not differ among conditions. These results provide evidence that GPi DBS does not affect pharyngeal swallowing function. Further, prospective, investigations are needed.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Weaver FM, Follett K, Stern M, et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced parkinson disease: A randomized controlled trial. JAMA. 2009;301:63–73. https://doi.org/10.1001/jama.2008.929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Won JH, Byun SJ, Oh B-M, et al. Risk and mortality of aspiration pneumonia in Parkinson’s disease: a nationwide database study. Sci Rep. 2021;11:6597. https://doi.org/10.1038/s41598-021-86011-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Plowman-Prine EK, Sapienza CM, Okun MS, et al. 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 

  4. Ramirez-Zamora A, Ostrem JL. Globus pallidus interna or subthalamic nucleus deep brain stimulation for Parkinson disease: a review. JAMA Neurol. 2018;75:367–72. https://doi.org/10.1001/jamaneurol.2017.4321.

    Article  PubMed  Google Scholar 

  5. Lee DJ, Lozano CS, Dallapiazza RF, Lozano AM. Current and future directions of deep brain stimulation for neurological and psychiatric disorders: JNSPG 75th Anniversary Invited Review Article. J Neurosurg. 2019;131:333–42. https://doi.org/10.3171/2019.4.JNS181761.

    Article  CAS  PubMed  Google Scholar 

  6. Asahi T, Inoue Y, Hayashi N, et al. Alleviation of dysphagia after deep brain stimulation: Results from a Parkinson’s disease patient. Mov Disord. 2012;27:325–6. https://doi.org/10.1002/mds.23899.

    Article  PubMed  Google Scholar 

  7. 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 

  8. Wolz M, Hauschild J, Fauser M, et al. Immediate effects of deep brain stimulation of the subthalamic nucleus on nonmotor symptoms in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:994–7. https://doi.org/10.1016/j.parkreldis.2012.05.011.

    Article  PubMed  Google Scholar 

  9. Zibetti M, Torre E, Cinquepalmi A, et al. Motor and nonmotor symptom follow-up in parkinsonian patients after deep brain stimulation of the subthalamic nucleus. ENE. 2007;58:218–23. https://doi.org/10.1159/000107943.

    Article  CAS  Google Scholar 

  10. Bejjani B-P, Gervais D, Arnulf I, et al. Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation. J Neurol Neurosurg Psychiatry. 2000;68:595–600. https://doi.org/10.1136/jnnp.68.5.595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Derrey S, Chastan N, Maltete D, et al. Impact of deep brain stimulation on pharyngo-esophageal motility: a randomized cross-over study. Neurogastroenterol Motil. 2015;27:1214–22. https://doi.org/10.1111/nmo.12607.

    Article  CAS  PubMed  Google Scholar 

  12. Kitashima A, Umemoto G, Tsuboi Y, et al. Effects of subthalamic nucleus deep brain stimulation on the swallowing function of patients with Parkinson’s disease. Parkinsonism Relat Disord. 2013;19:480–2. https://doi.org/10.1016/j.parkreldis.2012.10.023.

    Article  PubMed  Google Scholar 

  13. Kulneff L, Sundstedt S, Olofsson K, et al. Deep brain stimulation – effects on swallowing function in Parkinson’s disease. Acta Neurol Scand. 2013;127:329–36. https://doi.org/10.1111/ane.12019.

    Article  CAS  PubMed  Google Scholar 

  14. Olchik MR, Ghisi M, Ayres A, et al. The impact of deep brain stimulation on the quality of life and swallowing in individuals with Parkinson’s disease. Int Arch Otorhinolaryngol. 2018;22:125–9. https://doi.org/10.1055/s-0037-1603466.

    Article  PubMed  Google Scholar 

  15. Silbergleit AK, LeWitt P, Junn F, et al. Comparison of dysphagia before and after deep brain stimulation in Parkinson’s disease. Mov Disord. 2012;27:1763–8. https://doi.org/10.1002/mds.25259.

    Article  PubMed  Google Scholar 

  16. Lengerer S, Kipping J, Rommel N, et al. Deep-brain-stimulation does not impair deglutition in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:847–53. https://doi.org/10.1016/j.parkreldis.2012.04.014.

    Article  PubMed  Google Scholar 

  17. Xu C, Zhuang P, Hallett M, et al. Parkinson’s disease motor subtypes show different responses to long-term subthalamic nucleus stimulation. Front Hum Neurosci. 2018;12:365. https://doi.org/10.3389/fnhum.2018.00365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Merola A, Zibetti M, Angrisano S, et al. Parkinson’s disease progression at 30 years: a study of subthalamic deep brain-stimulated patients. Brain. 2011;134:2074–84. https://doi.org/10.1093/brain/awr121.

    Article  PubMed  Google Scholar 

  19. Krause M, Fogel W, Mayer P, et al. Chronic inhibition of the subthalamic nucleus in Parkinson’s disease. J Neurol Sci. 2004;219:119–24. https://doi.org/10.1016/j.jns.2004.01.004.

    Article  CAS  PubMed  Google Scholar 

  20. Fagbami OY, Donato AA. Stridor and dysphagia associated with subthalamic nucleus stimulation in Parkinson disease: case report. J Neurosurg. 2011;115:1005–6. https://doi.org/10.3171/2011.7.JNS11602.

    Article  PubMed  Google Scholar 

  21. Rosenbek JC, Robbins JA, Roecker EB, et al. A penetration-aspiration scale. Dysphagia. 1996;11:93–8. https://doi.org/10.1007/bf00417897.

    Article  CAS  PubMed  Google Scholar 

  22. Troche MS, Brandimore AE, Foote KD, et al. Swallowing outcomes following unilateral STN vs. GPi surgery: a retrospective analysis Dysphagia. 2014;29:425–31. https://doi.org/10.1007/s00455-014-9522-0.

    Article  PubMed  Google Scholar 

  23. McHorney CA, Bricker DE, Kramer AE, et al. The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: I. Conceptual foundation and item development Dysphagia. 2000;15:115–21. https://doi.org/10.1007/s004550010012.

    Article  CAS  PubMed  Google Scholar 

  24. Henry KA, Singh R, Zhang N, et al. Effect of STN/GPi DBS on swallowing function in Parkinson’s disease as assessed by Video fluoroscopy: A retrospective study. Parkinsonism Relat Disord. 2022;103:136–40. https://doi.org/10.1016/j.parkreldis.2022.08.017.

    Article  PubMed  Google Scholar 

  25. Hariz MI, Rehncrona S, Quinn NP, et al. Multicenter study on deep brain stimulation in Parkinson’s disease: an independent assessment of reported adverse events at 4 years. Mov Disord. 2008;23:416–21. https://doi.org/10.1002/mds.21888.

    Article  PubMed  Google Scholar 

  26. Anderson VC, Burchiel KJ, Hogarth P, et al. Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease. Arch Neurol. 2005;62:554–60. https://doi.org/10.1001/archneur.62.4.554.

    Article  PubMed  Google Scholar 

  27. Odekerken VJ, van Laar T, Staal MJ, et al. Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): a randomised controlled trial. The Lancet Neurology. 2013;12:37–44. https://doi.org/10.1016/S1474-4422(12)70264-8.

    Article  PubMed  Google Scholar 

  28. Troche MS, Brandimore AE, Hegland KW, et al. Tailored deep brain stimulation optimization for improved airway protective outcomes in Parkinson’s disease. Interdiscip Neurosurg. 2016;5:3–5. https://doi.org/10.1016/j.inat.2016.03.003.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Aldridge D, Theodoros D, Angwin A, Vogel AP. Speech outcomes in Parkinson’s disease after subthalamic nucleus deep brain stimulation: A systematic review. Parkinsonism Relat Disord. 2016;33:3–11. https://doi.org/10.1016/j.parkreldis.2016.09.022.

    Article  PubMed  Google Scholar 

  30. Follett KA, Weaver FM, Stern M, et al (2010) Pallidal versus Subthalamic Deep-Brain Stimulation for Parkinson’s Disease. In: https://doi.org/10.1056/NEJMoa0907083. https://www.nejm.org/doi/https://doi.org/10.1056/NEJMoa0907083. Accessed 18 Jun 2021

  31. Chiu SY, Tsuboi T, Hegland KW, et al. Dysarthria and speech intelligibility following Parkinson’s disease globus pallidus internus deep brain stimulation. J Parkinson’s Dis. 2020;10:1493–502. https://doi.org/10.3233/JPD-202246.

    Article  Google Scholar 

  32. Østergaard K, Sunde N, Dupont E. Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson’s disease and motor fluctuations. Mov Disord. 2002;17:693–700. https://doi.org/10.1002/mds.10188.

    Article  PubMed  Google Scholar 

  33. Pötter-Nerger M, Volkmann J. Deep brain stimulation for gait and postural symptoms in Parkinson’s disease. Mov Disord. 2013;28:1609–15. https://doi.org/10.1002/mds.25677.

    Article  PubMed  Google Scholar 

  34. George RJS, Nutt JG, Burchiel KJ, Horak FB. A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology. 2010;75:1292–9. https://doi.org/10.1212/WNL.0b013e3181f61329.

    Article  Google Scholar 

  35. Xie T, Padmanaban M, Bloom L, et al. Effect of low versus high frequency stimulation on freezing of gait and other axial symptoms in Parkinson patients with bilateral STN DBS: A mini-review. Transl Neurodegener. 2017. https://doi.org/10.1186/s40035-017-0083-7.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Xie T, Vigil J, MacCracken E, et al. Low-frequency stimulation of STN-DBS reduces aspiration and freezing of gait in patients with PD. Neurology. 2015;84:415–40. https://doi.org/10.1212/WNL.0000000000001184.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Karl JA, Ouyang B, Goetz S, Metman LV. A novel DBS paradigm for axial features in Parkinson’s disease: A randomized crossover study. Mov Disord. 2020;35:1369–78. https://doi.org/10.1002/mds.28048.

    Article  CAS  PubMed  Google Scholar 

  38. Xie T, Bloom L, Padmanaban M, et al. Long-term effect of low frequency stimulation of STN on dysphagia, freezing of gait and other motor symptoms in PD. J Neurol Neurosurg Psychiatry. 2018;89:989–94. https://doi.org/10.1136/jnnp-2018-318060.

    Article  PubMed  Google Scholar 

  39. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992;55:181–4. https://doi.org/10.1136/jnnp.55.3.181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Donohue C, Robison R, DiBiase L, et al. Comparison of validated videofluoroscopic outcomes of pharyngeal residue: Concordance between a perceptual, ordinal, and bolus-based rating scale and a normalized pixel-based quantitative outcome. J Speech Lang Hear Res. 2022;65:2510–7. https://doi.org/10.1044/2022_JSLHR-21-00659.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Bhutada AM, DeyMartin -Harris Bonnie, (Focht ) Garand Kendrea L R. Factors influencing initiation of pharyngeal swallow in healthy adults. Am J Speech Lang Pathol. 2020;29:1956–64. https://doi.org/10.1044/2020_AJSLP-20-00027.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Okun MS, Fernandez HH, Wu SS, et al. Cognition and mood in Parkinson’s disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: The COMPARE trial. Ann Neurol. 2009;65:586–95. https://doi.org/10.1002/ana.21596.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Molfenter SM, Steele CM. Kinematic and temporal factors associated with penetration–aspiration in swallowing liquids. Dysphagia. 2014;29:269–76. https://doi.org/10.1007/s00455-013-9506-5.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Hutcheson KA, Barrow MP, Barringer DA, et al. Dynamic Imaging Grade of Swallowing Toxicity (DIGEST): scale development and validation. Cancer. 2017;123:62–70. https://doi.org/10.1002/cncr.30283.

    Article  PubMed  Google Scholar 

  45. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biom. 1977;33:159–74. https://doi.org/10.2307/2529310.

    Article  CAS  Google Scholar 

  46. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63. https://doi.org/10.1016/j.jcm.2016.02.012.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Daggett A, Logemann J, Rademaker A, Pauloski B. Laryngeal penetration during deglutition in normal subjects of various ages. Dysphagia. 2006;21:270–4. https://doi.org/10.1007/s00455-006-9051-6.

    Article  PubMed  Google Scholar 

  48. Steele CM, Peladeau-Pigeon M, Barbon CAE, et al. Reference values for healthy swallowing across the range from thin to extremely thick liquids. J Speech Lang Hear Res. 2019;62:1338–63. https://doi.org/10.1044/2019_JSLHR-S-18-0448.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Humbert IA, Sunday KL, Eleni K, et al. Swallowing kinematic differences across frozen, mixed, and ultrathin liquid boluses in healthy adults: age, sex, and normal variability. J Speech Lang Hear Res. 2018;61:1544–59. https://doi.org/10.1044/2018_JSLHR-S-17-0417.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Chuck Jacobson, IV, for his assistance with querying the UF INFORM database.

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This research did not receive specific grant funding from any agencies.

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by MSH, NH, and JW. The first draft of the manuscript was written by MSH, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to May Smith-Hublou.

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Smith-Hublou, M., Herndon, N., Wong, J.K. et al. Impacts of Deep Brain Stimulation of the Globus Pallidus Internus on Swallowing: A Retrospective, Cross-Sectional Study. Dysphagia (2024). https://doi.org/10.1007/s00455-023-10660-4

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