Deep brain stimulation in Tourette’s syndrome: evidence to date

Figures & data

Figure 1 Diagram showing some of the possible clinical evolution that can be interpreted as natural history of TS or outcome from non-surgical therapeutic interventions based on YGTSS as a severity measure. This diagram intends to illustrate the current indications for DBS according to earlier and latest criteria. (A) Clinical resolution of TS symptoms. (B) Presence of tics that do not resolve spontaneously or are kept stable under non-surgical treatments. (C) Classical indication for DBS based on the severity of disease and age (18 years). (D) Latest proposed indication for DBS based on severity as a determinant factor even before 18 years of age.

Abbreviations: DBS, deep brain stimulation; TS, Tourette’s syndrome; YGTSS, Yale Global Tic Severity Scale.

Table 1 Clinical criteria for the indication of DBS in Tourette’s syndrome

	2006 guidelines	2015 MDS guidelines
Diagnosis	DSM-IV diagnosis of TS by expert clinician	DSM-V diagnosis of TS by expert clinician
Age	≥25 years old	Age is not a strict criteria * In patients ≤18 years old, a local ethics committee should be involved
Tic severity (measures)	A. Severe tic disorder with functional impairment B. Scales: YGTSS >35/50 C. Document with standardized video assessment	A. Severe tic disorder with functional impairment B. Scales: YGTSS >35/50 C. Document with standardized video assessment
Neuropsychiatric comorbidities	A. Tics as the most disable symptom B. Stable and treated comorbid conditions C. Scales: valid rating scales when available	A. Tics as the most disable symptom B. Stable and treated comorbid conditions C. Scales: valid rating scales when available
Refractoriness to conventional and optimal treatment	A. Failed treatment trials from three pharmacological classes: A.1: alpha-adrenergic agonist A.2: two dopamine antagonists (typical and atypical) A.3: benzodiazepine B. Evaluated for suitability of behavioral interventions for tics	A. Failed treatment trials from three pharmacological classes: A.1: alpha-adrenergic agonist A.2: two dopamine antagonists (typical and atypical) A.3: a drug from at least one additional class (eg, clonazepam, tetrabenazine) B. CBIT should be offered
Comorbid medical disorders	Stable for 6 months before DBS	Stable for 6 months before DBS
Psychosocial factors	A. Adequate social support without acute or subacute psychosocial stressors B. Active involvement with psychological interventions when necessary	A. Adequate social support without acute or subacute psychosocial stressors B. Active involvement with psychological interventions when necessary C. Caregiver available to accompany patient for frequent follow-up D. Psychogenic tics, embellishment, factitious symptoms, personality disorders, and malingering must be recognized and addressed
SI/HI	Not specifically addressed	Documentation of no active SI/HI for 6 months before surgery

Notes:

* Guideline changes in clinical indication criteria for DBS in Tourette’s Sindrome (modified from Schrock et al, 2015¹⁵).

Abbreviations: DBS, deep brain stimulation; SI/HI, suicidal/homicidal ideation; TS, Tourette’s syndrome; YGTSS, Yale Global Tic Severity Scale; CBIT, comprehensive behavioral intervention for tics.

Table 2 Summary of the studies: level III evidence

Study	Patients (n)	Follow-up (months)	Target	Outcomes
Maciunas et al, 2007^Citation17	5	3	Centromedian-parafascicular and ventralis oralis complex of the thalamus	Three of five patients showed improvement: mean pre-op YGTSS – 37.2, 3-mo score – 28.2
Welter et al, 2008^Citation77	3	20–60	Thalamus CM-Pf and GPi	30%–64% total YGTSS, 37%–41% tic severity subscale with CM-Pf; 65%–96%, 67%–90% with GPi; 43%–76%, 16%–70% with combined; recurrence of tics during sham but 32% improvement in 1 patient Crossover study of CM-Pf vs GPi vs combined vs sham(2 months per stimulation condition)
Porta et al, 2009^Citation61	15	24	Centromedian-parafascicular and ventralis oralis complex of the thalamus	5% improvement in tic scores. No deleterious effect on cognition, improvement in behavioral ratings
Kaido et al, 2011^Citation97	3	12	Thalamus	YGTSS decreased from 42.7±2.7 (before DBS) to 26.0±1.7 (1 year after DBS)
Ackermans et al, 2011^Citation18	6	3, 6, 12	Thalamus	Improvement (37%) on the YGTSS scale (mean 41.1±5.4 vs 25.6±12.8, P=0.046) After 1 year: significant improvement (49%) on the YGTSS scale (mean 42.2±3.1 vs 21.5±11.1, P=0.028) when compared with preoperative assessments
Okun et al, 2013^Citation116	5	6	Centromedian-parafascicular and ventralis oralis complex of the thalamus	YGTSS decreased by 17.8 points (P=0.01), MRVRS decreased by 5.8 points (P=0.01)
Motlagh et al, 2013^Citation72	8	6–107	Thalamus (5) and GPi (3) Two in the sensorimotor portion and one in limbic portion	YGTSS decreased by 0–72%
Dong et al, 2012^Citation70	1	22 with DBS 26 without DBS	GPi	66.7% improvement
Schoenberg et al, 2015^Citation25	5	5	Thalamus	24%
Huys et al, 2016^Citation63	8	12	Ventral anterior and ventrolateral motor parts of the thalamus	YGTSS motor, impairment, and total scores decreased by 51, 60, and 58%, respectively, compared to baseline MRVRS score decreased by 58% Significant improvement in quality of life and global functioning measures were noted
Kefalopoulou et al, 2015^Citation19	15	6 months blinded and then 36 months unblinded	GPi (anteromedial location)	15.3%–40.1% YGTSS decreased by 12.4 between on and off states in the blinded phase (P=0.048), YGTSS decreased by 23.8–48.9 points (P<0.0001) between baseline and open-label phase
Servello et al, 2016^Citation98	48	24	Thalamus – 42 aGPi – 2 NA – 4	78% of cases with >50% of improvement
Rossi et al, 2016^Citation56	5	24	Thalamus CM-Pf	40%
Welter et al, 2017^Citation76	16	3	aGPi	No significant difference in YGTSS score

Note: Summary of the main published studies on DBS for the treatment of tics and Tourette’s syndrome.

Abbreviations: YGTSS, Yale Global Tic Severity Scale; CM-Pf, centromedian-parafascicular-thalamic complex; GPi, globus pallidus internus; aGPi, anteromedial GPi; DBS, deep brain stimulation; NA, nucleus accumbens; MRTRSS, Modified Rush Tic Rating Scale Score total score.

Table 3 Summary of studies: level IV evidence

Study	Patients (n)	Follow-up (months)	Target	Outcome
Vandewalle et al, 1999^Citation13	1	12	Thalamus	Total symptomatic improvement
Van der Linden et al, 2002	1	6	Medial thalamus and GPi	80% Improvement with thalamus at high intensities, 95% with GPi at lower intensities at 1 wk; GPi connected to implantable pulse generator (IPG), with similar results at 6 mo
Visser-Vandewalle et al, 2003^Citation64	3	8–60	Thalamus	Improvement of motor and vocal severe tics
Houeto et al, 2005^Citation99	1	3, 5, 7, 9, 10	CM-Pf and GPi	65% total improvement on YGTSS, 77% improvement on RVBTS after CM-Pf; 65% total impr on YGTSS, 67% impr on RVBTS after GPi. Return to the baseline with sham Stim; 70% total impr on YGTSS, 76% improvement on RVBTS after CM-Pf + GPi.
Flaherty et al, 2005^Citation82	1	18	ALIC/NA	Symptomatic improvement
Diederich et al, 2005^Citation65	1	14	pGPi	71.6% tic/min (on videotape) at 7 mo, 84.6% at 14 mo; 66.0% tic increase at 14 mo “off”; 47.0% total improvement on YGTSS (44.2% tic severity subscale); improved premonitory urges – recurrence at 7 mo “off”
Gallagher et al, 2006^Citation100	1	Non-disclosed	GPi	Improvement
Ackermans et al, 2006^Citation78	2	12	CM, Spv, Voi in patient 1 GPi in patient 2	85.0% (tics/min on videotape) in patient 1, 92.9% in patient 2; minor tics remained in both patients; acute increase and decrease of tics during “off” and “on,” respectively
Vilela Filho et al, 2007^Citation85	2	23	GPe	Symptomatic improvement
Shahed et al, 2007^Citation27	1	6	GPi posteroventral	76.0% motor, 68.0% phonic tics (84.4% total on YGTSS); 21.4% RVBTRS
Bajwa et al, 2007^Citation59	1	1, 4, 6, 14, 20, 24	CM, Spv, Voi	66.2% YGTSS tic subscale; 98.0% reduced tic frequency via hand-held counter
Kuhn et al, 2007^Citation81	1	30	ALIC/NA	41.1% total on YGTSS, 50% RVBTRS at 30 mo
Zabek et al, 2008^Citation80	1	Baseline, at 6 and 28	Right NA	26.7% at 1 wk, 74.2% at 6 mo, 79.7% at 28 mo (tics/15 min via videotape); 50% tics in “off”
Shields et al, 2008^Citation101	1	18	VS/VC, thalamus	45%
Khun et al, 2008^Citation102	1	10	VS/VC	19.8% total on YGTSS at 1 mo, 51.9% at 10 mo; coprolalia nearly resolved
Dehning et al, 2008^Citation66	1	12	GPi	66.3% total on YGTSS at 6 wk, 88.0% at 1 y (tics abolished)
Servello et al, 2008^Citation60	18	3–18	Centromedian-parafascicular (CM-Pf) and ventralis oralis complex of the thalamus	YGTSS decreased from 33–48 to 7–22
Neuner et al, 2009^Citation83	1	36	NA, ALIC	46.0% at 3 mo, 44.0% at 36 mo, 40% at 58 mo (total YGTSS), 60%, 58%, 57% (RVBTRS)
Servello et al, 2009^Citation87	4	44/8–51	Internal capsule/NA in patients with centromedian-parafascicular and ventralis oralis complex of the thalamus (except one patient with only internal capsule/NA leads)	Two patients showed at best mild improvement in OCD and tic scores, two showed more clinically significant improvement in OCD scores and functionality, with limited effect on tics
Vernaleken et al, 2009^Citation36	1	Non-disclosed	GPi, CM-Pf, DM	No clinical improvement with GPi; 35.9% total on YGTSS (22.2% motor and 40.0% vocal tics) with CM-Pf/DM
Kuhn et al, 2009^Citation103	6	3–18	NA (n=2); GPi (n=2); thalamus (n=1); caudate (n=1)	50% improvement n=3; 50% in N=2; non response in n=1 during
Dueck et al, 2009^Citation104	1	12	GPi	Improvement in YGTSS scores, but not substantial overall
Foltynie et al, 2009^Citation105	1	Non-disclosed	GPi	88.7% motor and 90% vocal tics/5 min at 3 and 6 mo; reemergence of tics during “off” and of vocal tics when trying to speak; inner tension remained
Martinez-Torres et al, 2009^Citation79	1	12	STN	89% at 6 mo, 97% at 1 y (tics/10 min)
Ackermans et al, 2010^Citation58	2	120/60 12	Centromedian-parafascicular and ventralis oralis complex of the thalamus	YGTSS decreased from a mean of 42.3 prior to surgery to 21.5 on 1-y follow-up, P=0.028
Marceglia et al, 2010^Citation106	7	24	CM-Pf, Vop	33% Improvement in YGTSS (6 mo-2 y follow-up) improvement in motor scale
Burdick et al, 2010^Citation84	1	30	VS/VC	No improvement in tics, 120.0% (RVBTRS) and 115.2% (total YGTSS) at 6 mo
Lee et al, 2011^Citation107	1	18	Thalamus (CM-Pf)	81% improvement in total tics count and 58% improvement on YGTSS
Martínez-Fernández et al, 2011^Citation75	5	3–24	GPi (two patients with anteromedial location, two patients with posterolateral location, one patient initially with posterolateral switched after 18 mo to anteromedial location)	Mean YGTSS was 77.8 at baseline and 54.2 at last follow-up, mean MRVRS was 28.3 at baseline and 15.7 at last follow-up, Tourette Sindrome Quality of Life was 61.7 at baseline and 28.5 at last follow-up
Dehning et al, 2011^Citation71	4	5–48	GPi (posteroventrolateral location)	Two patients responded with >80% reduction in tics, two patients did not respond
Kuhn et al, 2011^Citation108	2	12	Thalamus (CM-Pf)	↑100%/67%
Savica et al, 2012^Citation23	3	12	Thalamus (CM-Pf)	↑70%
Dong et al, 2012^Citation70	2	12	GPi D	↑58.5%/53.1%
Cannon et al, 2012^Citation74	11	4–30	GPi (anteromedial location)	One patient did not respond; mean YGTSS was 84.45 before surgery and 42.55 at 3 mo, mean TSQOL was 39.09 before surgery and 79.09 at 3 mo
Maling et al, 2012^Citation40	5	6	Centromedian-parafascicular and ventralis oralis complex of the thalamus	YGTSS decreased by 1%–41%; noted correlation between gamma-band activity change and YGTSS change after DBS
Hwynn et al, 2012^Citation109	1	1, 3, 6, 9, 12, 24, 36	GPi	Improvement in tics and dystonia
Porta et al, 2012^Citation62	18	60–72	Centromedian-parafascicular and ventralis oralis complex of the thalamus	Mean YGTSS was 80.83 prior to surgery and 22.11 at the extended follow-up (P<0.001) 72.6% Improvement.
Piedimonte et al, 2013^Citation86	1	6	GPe	↑70.5%
Dehning et al, 2014^Citation67	6	12–60	GPi (posteroventrolateral location)	Two patients were non-responders, mean YGTSS was 90.2 prior to surgery and 29.5 at last follow-up (P=0.001); TSQOL was 88.75 prior to surgery and 7.75 at last follow-up (one person did not fill TSQOL)
Huasen et al, 2014^Citation110	1	12	GPi anteromedial	55%
Zhang et al, 2014^Citation24	13	13–80	GPi (posterolateral location)	Mean YGTSS decreased by 52.1% at last follow-up, mean TSQOL improved by 45.7% at last follow-up
Sachdev et al, 2014^Citation22	17	48	GPi anteromedial	38%
Patel & Jimenez-Shahed, 2014^Citation111	1	14	GPi	47%
Zekaj et al, 2015^Citation112	1	72	Thalamus	58.2% improvement during “off” condition
Testini et al, 2016^Citation113	12	Median 26	Thalamus (CM-Pf)	54% improvement
Smeets et al, 2016^Citation68	5	1–12–38	Anterior internal globus pallidus	YGTSS was significantly lower than the preoperative score (42.2±4.8 vs 12.8±3.8, P=0.043). No significant difference in the secondary outcomes was found; however, there was an improvement at an individual level for obsessive–compulsive behavior
Cury et al, 2016^Citation26	1	18	Thalamus (CM-Pf)	70.5%
Zhang et al, 2014^Citation24	24	12	GPi	56%
Dwarakanath et al, 2017^Citation114	1	Non-disclosed	GPi anteromedial	72%
Hauseux et al, 2017^Citation88	3	52	GPi posteroventral + GPe GPi posteroventral + GPi posteroventral + thalamus (CM-Pf) + NA	Symptoms improvement
Smeets et al, 2017^Citation115	7	12–78	Thalamus (CM-Pf)	Improvement from 9% to 88.1%

Note: Summary of the main published studies on DBS for the treatment of tics and Tourette’s syndrome.

Abbreviations: mo, month; y, year; wk, week; YGTSS, Yale Global Tic Severity Scale; CM-Pf, centromedian-parafascicular-thalamic complex; GPi, globus pallidus internus; DBS, deep brain stimulation; STN, subthalamic nucleus; GPe, globus pallidus externus; NA, nucleus accumbens; ALIC, anterior internal capsule; VS/VC, ventral striatum/ventral capsule; pGPi, posteroventral GPi; OCD, obsessive–compulsive disorder.

Figure 2 Targets proposed for DBS treatment in Tourette’s syndrome: (A) anterior limb of internal capsule/accumbens; (B) bilateral centromedian-parafascicular complex targeted in an anterolateral thalamic view (basal, anterior, and lateral thalamic views of the right thalamus are displayed for localization within the thalamus); and (C) different parts of GPi. Electrode 1 is located in the posteroventrolateral GPi and electrode 2 is located in the anteromedial GPi. The 3D representations are histological postmortem reconstructions of the nuclei from the University of São Paulo – Würzburg Atlas of the Human Brain (Alho et al, 2018⁹⁶).

Abbreviations: ACC, accumbens; Cau, caudate nucleus; GPi, globus pallidus internus; GPe, globus pallidus externus; Put, putamen; ALIC, anterior limb of internal capsule; CM-Pf, centromedian-parafascicular-thalamic complex; LG, lateral thalamic group; STN, subthalamic group.

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