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The effects of deep brain stimulation on speech intelligibility in persons with essential tremor
Umeå University, Faculty of Medicine, Department of Clinical Sciences, Speech and Language Therapy.ORCID iD: 0000-0002-7626-2889
Umeå University, Faculty of Medicine, Department of Pharmacology and Clinical Neuroscience, Clinical Neuroscience.ORCID iD: 0000-0001-9413-6950
Umeå University, Faculty of Medicine, Department of Clinical Sciences, Speech and Language Therapy.ORCID iD: 0000-0003-3373-0934
Neurovetenskap och fysiologi, Sektionen för hälsa och rehabilitering, Göteborgs universitet.ORCID iD: 0000-0003-3461-7618
2020 (English)In: Journal of Speech, Language and Hearing Research, ISSN 1092-4388, E-ISSN 1558-9102, Vol. 63, no 2, p. 456-471Article in journal (Refereed) Published
Abstract [en]

Purpose: To investigate how deep brain stimulation (DBS) of the caudal zona incerta (cZi) affects speech intelligibility in persons with essential tremor (ET).

Method: Thirty-five participants were evaluated: off stimulation, on chronic stimulation optimized to alleviate tremor, and during unilateral stimulation at increasing amplitude levels. At each stimulation condition, the participants read 10 unique nonsense sentences from the Swedish Test of Intelligibility. Two listeners, blinded to stimulation condition, transcribed all recorded sentences orthographically in a randomised procedure. A mean speech intelligibility score for each patient and stimulation condition was computed, and comparisons were made between scores off- and on stimulation.

Results: Chronic cZi-DBS had no significant effect on speech intelligibility, and there was no difference in outcome between bilateral and unilateral treatments. During unilateral stimulation at increasing amplitudes, nine participants demonstrated deteriorating speech intelligibility. These nine participants were on average older and had more superior contacts activated during the evaluation compared with the participants without deterioration.

Conclusions: Chronic cZi-DBS, optimized for tremor suppression, does not generally affect speech intelligibility in persons with ET. Furthermore, speech intelligibility may be preserved in many individuals, even when stimulated at high amplitudes. Adverse effects of high-amplitude unilateral stimulation observed in this study were associated with stimulation originating from a more superior location, as well as with the participants’ age. These results, highlighting age and stimulation location as contributing to speech intelligibility outcomes were, however, based on a limited number of individuals experiencing adverse effects with high-amplitude stimulation and should, therefore, be interpreted with caution.

Place, publisher, year, edition, pages
American Speech-Language-Hearing Association, 2020. Vol. 63, no 2, p. 456-471
Keywords [en]
caudal zona incerta, deep brain stimulation, essential tremor, posterior subthalamic area, speech intelligibility
National Category
Neurology
Research subject
Neurosurgery
Identifiers
URN: urn:nbn:se:umu:diva-166782DOI: 10.1044/2019_JSLHR-19-00014PubMedID: 32091953Scopus ID: 2-s2.0-85081158509OAI: oai:DiVA.org:umu-166782DiVA, id: diva2:1381990
Available from: 2019-12-30 Created: 2019-12-30 Last updated: 2020-03-30Bibliographically approved
In thesis
1. Impact of deep brain stimulation in the caudal zona incerta on voice tremor and speech in persons with essential tremor
Open this publication in new window or tab >>Impact of deep brain stimulation in the caudal zona incerta on voice tremor and speech in persons with essential tremor
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Objectives: Deep brain stimulation (DBS) is a symptomatic treatment for people with essential tremor (ET) who have unsatisfactory tremor relief with pharmacological treatment alone. A common symptom of ET is voice tremor, but only about 50% of patients with voice tremor get a satisfactory result with DBS. Moreover, stimulation-induced adverse effects on speech are often reported, especially with bilateral stimulation. In recent years, the caudal zona incerta (cZi) has been highlighted as a particularly efficient DBS-target for tremor; however, less is known about the effects of cZi-DBS on voice and speech. The aims of this thesis were to (i) describe how voice tremor and speech production are affected by habitual cZi-DBS optimized to treat the motor symptoms of ET, (ii) investigate how voice tremor and speech production are affected by unilateral cZi-stimulation at increasing amplitudes, with a particular focus on high-amplitude stimulation, and (iii) explore the extent to which patient characteristics and DBS related factors, such as electrode location and stimulation settings, influence the outcome.

Methods: This thesis comprises two different study protocols. Study I was a retrospective study of 19 patients with ET and voice tremor, and DBS effects on voice tremor were evaluated from clinical assessments made at baseline and 1, 3, and 5 years after surgery, respectively. Studies II-V included 37 persons with ET, and DBS effects on voice tremor and speech production were evaluated off- and on habitual stimulation, as well as in an experimental protocol with unilateral stimulation at increasing amplitudes (up to a maximum of 4.5V). Voice tremor (study II, III) was assessed by two listeners using the Visual Sort and Rate (VISOR) method. Speech intelligibility (study IV) was estimated from orthographic transcriptions of nonsense sentences made by two speech-language pathology students. Speech function, including articulation and voice quality (study V) were analysed in 14 participants and assessed by two speech-language pathologists using VISOR. Voice and speech outcomes following the experimental stimulation condition were evaluated in relation to the location of the active electrode contacts.

Results: Habitual cZi-DBS reduced voice tremor at all examinations and did not affect speech production on the group-level. By contrast, during unilateral high-amplitude stimulation, more negative effects on speech were noted, and the proportion of individuals with affected speech more than doubled at maximal amplitude stimulation compared with habitual cZi-DBS (40% compared to 17%). While most of these adverse effects were mild in general, a few participants exhibited more severe impairments of high-amplitude stimulation, especially on speech intelligibility and articulation. There were also cases in which high-amplitude stimulation worsened voice tremor or even induced the symptom. As for the contribution of electrode location, a deeper and more posterior stimulation origin were found to yield the most efficient voice tremor reduction, more medially located electrodes were associated with affected articulation, whereas deteriorated speech intelligibility was related to stimulation originating from a more superior location.

Conclusions: cZi-DBS is relatively safe in the sense that adverse effects on speech production are rarely seen during stimulation with the clinical settings. Furthermore, voice tremor can be expected to improve, both short- and long- term, although not always to such an extent that the symptom is alleviated completely. However, by increasing the stimulation amplitude beyond the clinical setting, one increases the risk of inducing unwanted speech-related effects and worsen voice tremor. Thus, it appears as though the challenge in the postoperative management of the DBS treatment lies in maintaining the therapeutic effect while still keeping the stimulation amplitude at a low level. The combined results of this thesis indicate that the best outcome for voice and speech might be achieved by stimulating from the posterior-inferior-lateral part of the cZi.

Abstract [sv]

Essentiell tremor är en vanlig rörelsestörningssjukdom som kännetecknas av tremor (skakningar) främst i armar och händer, men det är även vanligt att rösten drabbas. Djup hjärnstimulering (deep brain stimulation, DBS) är en kirurgisk behandlingsmetod som visats vara mycket effektiv på tremor överlag, dock är resultaten gällande rösttremor mer varierande. Dessutom är talpåverkan en vanlig bieffekt av DBS, speciellt vid bilateral stimulering. I denna avhandling har DBS i kaudala zona incerta (cZi) utvärderats gällande dess effekter på rösttremor och talproduktion hos personer med ET. Syftet med avhandlingen är att: (i) beskriva effekterna av kronisk cZi-DBS som optimerats för att behandla ET, (ii) utforska effekterna av unilateral stimulering vid successivt ökande amplituder (med ett särskilt fokus på högamplitudstimulering), samt (iii) undersöka vilka faktorer som kan tänkas påverka resultatet.

Delstudie 1 är en retrospektiv långtidsstudie av 19 patenter med ET som hade rösttremor innan DBS-behandling. Effekterna av DBS på rösttremor utvärderades från bedömningar gjorda vid uppföljningar 1, 3 samt 5 år efter operation. Delstudie 2-5 inkluderade 37 personer med ET och effekterna av DBS på rösttremor och talproduktion utvärderades utifrån bedömningar gjorda: 1) med DBS avstängd, 2) med kronisk cZi-DBS, samt 3) vid unilateral stimulering i en experimentell procedur med gradvis ökande amplituder (upp till maximalt 4.5V). Rösttremor (delstudie 2 och 3) bedömdes perceptuellt av två lyssnare. Talförståelighet (delstudie 4) beräknades som procent korrekt uppfattade ord utifrån ortografiska transkriptioner av nonsensmeningar som utfördes av två logopedstudenter. Talfunktion, inklusive artikulation och röstkvalitet hos 14 personer med ET (delstudie 5) bedömdes perceptuellt av två erfarna logopeder. Röst- och talresultat från den experimentella stimuleringsproceduren utvärderades också i förhållande till elektrodens anatomiska läge.

Resultaten visade att kronisk cZi-DBS inte hade några negativa effekter på talproduktion överlag. Kronisk cZi-DBS förbättrade också rösttremor genomgående, dock med en betydande individuell variation. Under unilateral högamplitudsstimulering visade sig däremot fler negativa effekter på såväl rösttremor som på talproduktion. Vid stimulering med den maximala amplitudnivån hade andelen individer med talpåverkan mer än fördubblats jämfört med den vid kronisk cZi-DBS (från 17 % till 40 %). Även om dessa negativa effekter var små generellt sett var det tydligt att enskilda individers tal drabbades mer än andras. Vad gäller betydelsen av elektrodens läge inom cZi visade det sig att ett djupare och mer posteriort läge var gynnsamt för rösttremor. För talproduktion var negativa effekter förknippade med ett mer medialt läge (för artikulation) samt ett högre läge (för talförståelighet).

Sammantaget tyder avhandlingens resultat på att cZi-DBS sällan orsakar negativa effekter på tal när patienten stimuleras med de kliniska inställningarna (optimerade för att behandla symptomen av ET). Dessutom kan rösttremor förväntas förbättras, både på kort och på lång sikt. Däremot kan talpåverkan och negativa effekter på rösttremor framkallas om stimuleringsamplituden höjs. Utmaningen i den postoperativa behandlingen ligger således i att kunna bibehålla den terapeutiska behandlingseffekten samtidigt som stimuleringsamplituden hålls ner. Våra resultat antyder också att det kan vara bäst för patienters röst och tal om stimuleringen utgår från ett djupare, mer posteriort och mindre medialt läge inom cZi-området.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, 2020. p. 67
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 2068
Keywords
caudal zona incerta, deep brain stimulation, essential tremor, speech function, speech intelligibility, speech production, voice tremor
National Category
Other Medical Sciences not elsewhere specified Neurosciences
Identifiers
urn:nbn:se:umu:diva-166784 (URN)978-91-7855-163-7 (ISBN)978-91-7855-162-0 (ISBN)
Public defence
2020-01-31, Sal A, psykiatriska kliniken, målpunkt F, plan 0, Norrlands universitetssjukhus, Umeå, 09:00 (English)
Opponent
Supervisors
Available from: 2020-01-10 Created: 2019-12-31 Last updated: 2020-01-07Bibliographically approved

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Sandström, LindaBlomstedt, PatricKarlsson, Fredrik

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