REVIEW

Tourette Syndrome Deep Brain Stimulation: A Review and Updated Recommendations Lauren E. Schrock, MD,1 Jonathan W. Mink, MD, PhD,2 Douglas W. Woods, PhD,3 Mauro Porta, MD,4 Dominico Servello, MD,5 Veerle Visser-Vandewalle, MD, PhD,6 Peter A. Silburn, MD,7 Thomas Foltynie, MRCP, PhD,8 Harrison C. Walker, MD,9 Joohi Shahed-Jimenez, MD,10 Rodolfo Savica, MD,1 Bryan T. Klassen, MD,11 Andre G. Machado, MD,12 Kelly D. Foote, MD,13 Jian-Guo Zhang, MD, PhD,14 Wei Hu, MD, PhD,11,14 Linda Ackermans, MD, PhD,15 Yasin Temel, MD, PhD,15 Zoltan Mari, MD,16 Barbara K. Changizi, MD,17 Andres Lozano, MD,18 M. Auyeung, MD,19 Takanobu Kaido, MD, PhD,20 Yves Agid, MD, PhD,21 Marie L. Welter, MD, PhD,22 Suketu M. Khandhar, MD,23 Alon Y. Mogilner, MD, PhD,24 Michael H. Pourfar, MD,24 Benjamin L. Walter, MD,25 Jorge L. Juncos, MD,26 Robert E. Gross, MD,27 Jens Kuhn, MD,28 James F. Leckman, MD,29 Joseph A Neimat, MD,30 Michael S. Okun, MD,13* on behalf of the and Tourette Syndrome Association International Deep Brain Stimulation (DBS) Database and Registry Study Group 1 Department of Neurology, University of Utah, Salt Lake City, Utah, USA Department of Neurology, University of Rochester Medical Center, Rochester, New York, USA 3 Department of Psychology, Texas A&M University, College Station, Texas, USA 4 Tourette Centre, IRCCS Galeazzi Hospital, Milan, Italy 5 Functional Neurosurgical Unit, IRCCS Galeazzi Milano, Milan, Italy 6 Department of Stereotactic and Functional Neurosurgery, University of Cologne, Cologne, Germany 7 Royal Brisbane and Women’s Hospital, School of Medicine, University of Queensland, Brisbane, Queensland, Australia 8 University College London Institute of Neurology, London, United Kingdom 9 Department of Neurology, University of Alabama Birmingham, Birmingham, Alabama, USA 10 Department of Neurology, Baylor College of Medicine, Houston, Texas, USA 11 Department of Neurology, Mayo Clinic, Rochester, Minnesota, USA 12 Center for Neurological Restoration, Neurological Institute, Cleveland Clinic, Cleveland, OH, USA 13 Departments of Neurology, Neurosurgery, and Psychiatry, University of Florida Center for Movement Disorders and Neurorestoration, Gainesville, Florida, USA 14 Department of Neurosurgery, Beijing Tiantan Hospital, Capital University of Medical Sciences, Beijing, China 15 Department of Neurosurgery, Maastricht University Medical Center, The Netherlands 16 Department of Neurology, Johns Hopkins University, Baltimore, Maryland, USA 17 Departments of Neurology and Psychiatry, The Ohio State University Wexner Medical Center, Ohio, USA 18 Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada 19 Department of Medicine, Pamela Youde Nethersole Eastern Hospital, Hong Kong, SAR China 20 Department of Neurosurgery, National Center Hospital, National Center of Neurology and Psychiatry (NCNP), Tokyo, Japan 21 -Salpe ^trie`re, Paris, France Institut du Cerveau et de la Moelle Epinie`re (ICM), CHU Pitie 22 pinie`re (CRICM), Universite  Pierre et Marie Curie-Paris 6, Paris, Centre de Recherche de l’Institut du Cerveau et de la Moelle e France 23 Northern California Kaiser Permanente, Surgical Movement Disorders Program, Sacramento, California, USA 24 Departments of Neurosurgery and Neurology, New York University, Langone Medical Center, New York, New York, United States of America 25 Movement Disorders Center, Neurological Institute, University Hospitals and Case Western Reserve University School of Medicine, South Euclid, Ohio, USA 26 Department of Neurology, Emory University School of Medicine, Atlanta, Georgia, USA 27 Department of Neurosurgery, Emory University School of Medicine, Atlanta, Georgia, USA 28 Department of Psychiatry and Psychotherapy, University of Cologne, Cologne, Germany 29 Child Study Center and the Yale Center for Clinical Investigation, Yale University School of Medicine, New Haven, Connecticut, USA 30 Department of Neurological Surgery, Vanderbilt University Medical Center, Nashville, Tennessee, USA 2

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*Correspondence to: Michael S. Okun, MD, 3450 Hull Road, Department of Neurology, Center for Movement Disorders and Neurorestoration, Gainesville, FL 32607, E-mail: [email protected] Funding agencies: Relevant conflicts of interest/financial disclosures: Nothing to report. Author roles may be found in the online version of this article. Received: 4 April 2014; Revised: 6 October 2014; Accepted: 8 October 2014 Published online 00 Month 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mds.26094

Movement Disorders, Vol. 00, No. 00, 2014

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ABSTRACT:

Deep brain stimulation (DBS) may improve disabling tics in severely affected medication and behaviorally resistant Tourette syndrome (TS). Here we review all reported cases of TS DBS and provide updated recommendations for selection, assessment, and management of potential TS DBS cases based on the literature and implantation experience. Candidates should have a Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM V) diagnosis of TS with severe motor and vocal tics, which despite exhaustive medical and behavioral treatment trials result in significant impairment. Deep brain stimulation should be offered to patients only by experienced DBS centers after evaluation by a multidisciplinary team. Rigorous preoperative and postoperative outcome measures of tics and associated comorbidities should be used. Tics and comorbid neuropsychiatric conditions should be optimally treated per current expert standards, and tics should be the major cause of disability. Psychogenic tics, embellishment, and malingering should be recog-

Tourette syndrome (TS) is a chronic neurodevelopmental disorder characterized by motor and phonic tics that by definition occur with a childhood onset.1 The syndrome is commonly associated with other neuropsychiatric comorbidities (eg, attention deficit hyperactivity disorder [ADHD], obsessive compulsive features [OCD], and other behavioral manifestations). In most TS cases, the motor manifestations can be managed using TS education, comprehensive behavioral intervention for tics (CBIT), or a variety of medications.2-4 The natural history of TS is that most patients will experience improvement of tics in late adolescence or early adulthood.5,6 However, a subset of patients will continue to experience disabling tics despite optimal medication and behavioral management. For severely affected patients, deep brain stimulation (DBS) has the potential to improve refractory and disabling symptoms.

Methods An experienced group of physicians participating in the Tourette Syndrome Association (TSA) International DBS Database/Registry, and also actively involved in managing TS DBS patients, reviewed the 2006 TSA guidelines7 and examined all reported cases of TS DBS. The TSA Database/Registry group accepted complete information sets on outcomes from TS DBS (database entry), as well as registration of cases performed with or without outcome information (registry entry). The group summarized the literature (Table 1) and based on their collective experience

2

Movement Disorders, Vol. 00, No. 00, 2014

nized and addressed. We have removed the previously suggested 25-year-old age limit, with the specification that a multidisciplinary team approach for screening is employed. A local ethics committee or institutional review board should be consulted for consideration of cases involving persons younger than 18 years of age, as well as in cases with urgent indications. Tourette syndrome patients represent a unique and complex population, and studies reveal a higher risk for postDBS complications. Successes and failures have been reported for multiple brain targets; however, the optimal surgical approach remains unknown. Tourette syndrome DBS, though still evolving, is a promising approach for a subset of medication refractory and severely affected C 2014 International Parkinson and Movement patients. V Disorder Society

K e y W o r d s : Tourette syndrome; DBS; guidelines; deep brain stimulation

with TS DBS provided suggested updates (Table 2) and a consensus opinion on the TSA recommendations put in place in 2006.7

Literature Review Deep brain stimulation is an established treatment for Parkinson’s disease (PD),8-12 essential tremor,13,14 dystonia,15-17 and obsessive-compulsive disorder,18,19 and has been granted either full Food and Drug Administration (FDA) approval (PD, essential tremor), or a humanitarian device exemption (FDA; dystonia, OCD) for each of these indications (in the United States). Many studies and position papers detail careful and meticulous techniques for screening patients for DBS,13,16,20-22 including a few reports for TS patients.23,24 General guidelines for selecting individual TS patients for DBS therapy and for managing them preoperatively and postoperatively will have the potential to improve risk–benefit ratios. The importance of rigorous preoperative assessment, patient selection, DBS team expertise and experience, as well as postoperative management has been demonstrated previously, especially when groups have studied cohorts of patients who have failed DBS therapy.25,26 Because TS is a childhood-onset disorder, often with complex clinical features, a waxing and waning course, and frequent neuropsychiatric comorbidities, the evaluation of patients has a greater level of complexity than many of the other current DBS indications. In 2005, the TSA hosted a meeting of physicians with experience and expertise in TS and DBS to

CM-Spv-Voi

Duits et al., 201239

1 (F)* enrolled 21 but didn’t complete previously reported trial31

8 (2F, 6M); *2F lost to follow-up

CM-Spv-Voi

Ackermans et al., 201130

21–48

17–46

15 (12M, 3F); *all previously reported62

CM-Pfc, Voa

1 (21)

1 (21)

Study Design

23 mo

12 mo

IV

IV

Level of Evidence

Case report

IV

Double-blind III randomized cross-over trial 3 6 mo, then 6 mo openlabel

Case series

3–18 mo Case series

7 (218 yrs) 24 mo

8 (2  18 yrs)

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

Porta et al., 200958

Sample size (n)

17–47

Target

Servello et al., CM-Pfc, Voa 18 (15M, 3F) 200861

Study

1. YGTSS—worse with DBS ON: Pre-op—42 Stim OFF—12 Stim ON—39

1. YGTSS 49% improvement 2. mRVTRS 35% improvement

1. YGTSS 52% mean improvement

1.YGTSS 64.7% mean improvement

Tic Outcome Measures

Target: Thalamic

Yes (9 with SIB; 3 No cervical myelopathy, 1 disc herniation, 2 unable to eat)

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

1. Y-BOCS: Preop—20 Stim OFF—8 Stim ON—7 2. CAARS: Pre-op—58 Stim OFF—42 Stim ON—45

Yes (lifethreatening)

No

1. Y-BOCS Yes No 31% mean improvement 2. STAI 33% mean improvement 3. BDI 26% mean improvement 4.VAS subjective social impairment 31% mean improvement 1. Y-BOCS—no change Yes (1 lifeYes 2. CAARS—no change threatening, lost 3. BDI (Dutch)—no to follow-up) change 4. BAI—no change 5. VAS for SIB—no change

None reported

Comorbidity Outcome Measures

TABLE 1. Review of reported TS DBS cases

(Continued)

1. Transient stim-induced vertigo & visual AE 2. Poor scalp incision healing due to repetitive touching; body shield required (n 5 1) 3. Abdominal hematoma (n 5 1) 4. Frequent programming required in many 1. 3 pts from previous cohort (n 5 18) were excluded: 2 pts requested removal of IPG and DBS was stopped 1 pt did poorly and required subsequent GPi DBS 1. Decreased energy levels, subjective gaze disturbance, negative impact on daily living in all pts 2. 1 small hemorrhage at lead tip—gaze palsy 3 6 mo, persistent nystagmus 3.1 IPG Infection 4. Severe complications, psychogenic symptoms, & eventual death in 1 pt lost to follow-up (see details below40) 1. Severe postoperative complications with psychogenic paroxysmal hypertonia, disturbances of consciousness, and mutism 2. No change with DBS OFF

Adverse Events Reported

Visser-Vande- CM-Spv-Voi walle et al., 200370

3 (3M); *1M 28,42,45 previously reported27

42

CM-Spv-Voi

Vandewalle et al., 199968

1 (M)

1 (M) *prev 45 reported70

CM-Spv-Voi

Ackermans et al., 200627

0

0

0

0

Case report

Case report

case report

Study Design

8 mo—5 Case series yrs

4 mo

1 yr

6 mo

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

1 (M) *previ- 39 ously reported31

Sample size (n)

CM-Spv-Voi

Target

Ackermans 200728

Study

IV

IV

IV

IV

Level of Evidence

3. BDI-II: Pre-op—12 Stim OFF—20 Stim ON—15 4. BAI Pre-op—32 Stim OFF—41 Stim ON—44 5. SIB (VAS) Pre-op—5.7 Stim OFF—0 Stim ON—8.9 None reported

Comorbidity Outcome Measures

Yes (headbanging)

No

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

No No 1. Videotaped tic fre- 1. Padua Inventory— quency (tics/min) by 2 Revised (obsession-comblinded raters pulsion rating) 85% reduction 62% better ON than OFF stim 1. Videotaped tic None reported No No frequency —Nearly 100% reduction (“except for some excessive eye blinking”) 1. Videotaped tic fre- None reported No (burning eye- No quency (tics/10min) lashes with cigarettes, break—72%—90% ing glass in reduction hands)

NA

Tic Outcome Measures

Target: Thalamic

TABLE 1. Continued

(Continued)

1. Reduced energy levels in all 3 2. Sexual dysfunction in 2 pts 3. 2 pts each required 3 revisions of IPG and extension wires due to traction pain 4.1 pt had lower scores on timed tasks on neuropsychological testing

Not reported

1. Hemorrhage at distal electrode tip --> vertical gaze palsy: subjective worsening with DBS ON 1. Decreased energy level 2. Sexual dysfunction

3. Somatoform disorder identified retrospectively 4. Pt died of dehydration, refusal to eat/drink @3 yrs postoperatively

Adverse Events Reported

Bajwa et al., CM-Spv-Voi 200731

1 (M)

48

18–34

5 (4M, 1F)

CM-Pf

Maciunas et al., 200749

0

1

0

Study Design

2 yrs

4 mo

IV

Level of Evidence

Case report

IV

Prospective III double-blind crossover trial; four 7-d randomized DBS conditions R/L, ON/OFF, and open-label 4-mo follow-up

6–10 yrs Case reports

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

2 (2M); *previ- 42, 45 ously reported27,28

Sample size (n)

CM-Spv-Voi

Target

Ackermans et al., 201029

Study

Comorbidity Outcome Measures

1. mRVTRS 40%-67% mean motor tic reduction 21%-70% mean vocal tic reduction 2. YGTSS 43.6% mean improvement 2 nonresponders with 4.3–260.9% tic exacerbation 3. TSSL 43% mean reduction 1.YGTSS 63.6% improvement

1. Y-BOCS 72.4% improvement 2. CGI “very much improved”

1. SF-36 (19% mean improvement) 2. VAS (53% mean improvement) 3. BDI-2* (60% mean improvement) 4. HAM-D* (29% mean improvement) 5. HAM-A* (51% mean improvement) 6. Y-BOCS* (44% mean improvement) *Trend toward improvement at 4 mo

1. Videotaped tic fre- None reported quency (tics/10min) by 3 blinded raters 78%-92.6% reduction

Tic Outcome Measures

Target: Thalamic

TABLE 1. Continued

Yes (only mean coordinates provided)

Yes (head-snap- No ping tics causing cervical myelopathy)

Not reported

No (breaking glass No in hands)

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

(Continued)

1. Although tics dramatically reduced, the head-snapping tics had only mild reduction in forcefulness and he had continued neurological deterioration due to myelopathy

1. Reduced energy levels in both pts 2. Both with hardwarerelated complications (traction of lead in neck) requiring multiple surgical revisions and local injections (previously described63) 3. Mild visual side effects (vertigo, blurry vison) in both 4. Sexual dysfunction in both 5. Increased aggression, social adaptation in 1 pt. 1. 1 pt had acute psychosis on day 28 of randomized phase— thought to be related to acute life stressors

Adverse Events Reported

Target

Sample size (n)

7 (6M, 1F) *many/all reported elsewhere (62)

CM-Pf, Voa

Marceglia et al., 201050

Servello et al., CM-Pfc, Voa 31 (25M, 6F,); (1 unilateral, *18 previ201063 excluded ously from reported(62) analysis) (4 additional pts received leads in multiple targets & 1 in ALIC/NA only)

1 (M)

CM-Pf, Voa

3 (2M, 1F)

Idris et al., 201043

Savica et al., CM-Pf 201260

Shields et al., CM* (ALIC 1 (F) 200867 leads previously removed)

Study

24

40

17–57

24–52

17–35

1 (24)

11

1

2 (17,17)

0

Case report

Case series

Case report

Study Design

IV

IV

IV

IV

Level of Evidence

3 mo-4 yr Case series (36 pt IV cohort; 6 excluded from analysis due to 100 Hz stimulation

Not reported

1. No severe adverse effects Not reported

1. Frequent visits in 1st few months for depression, vertigo, stomach aches; difficulty adjusting to new situation without tics. 1. Stimulation stopped due to lack of response (n 5 2) 2. Lead revision to a more posterior location was done in 1 nonresponder, without improvement

Adverse Events Reported

Target

1

GPe

2

1

11

Sample size (n)

GPe

Motlagh et al., pvGPi 201353

Filho et al., 200756 Piedimonte et al., 201357

Cannon et al., amGPi 201233

Study

2M (24, 42)

47 (M)

NA

1(24)

NA 0

8M (22–50);3F 2 (18,22) (18–34)

Study Design

IV

Level of Evidence

IV

Case report IV (abstract only) Case report IV

8–51 mo Case series

2 yrs

23 mo

4–30 mo Case series

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

No

No

4. GAF—(36% improvement @ 6mo) Yes 1. YGTSS—20%-44% 1. Y-BOCS—no Yes (2 of 2; improvement significant change punching self, 2. HDRS—no change to neck-snapping mild improvement tics 1 cervical 3. HARS—slight spine injury) improvement

No

Not reported

1. Y-BOCS (59% mean Yes (requiring 24- No improvement) hr monitoring to prevent head 2. HDRS (74% injury) mean improvement) 3. GTS-QLS—significant improvement (102% mean improvement) 4. GAF (57% mean improvement)

Comorbidity Outcome Measures

1. YGTSS—81 % 1. Y-BOCS—84% reduction reduction 1. YGTSS 1. Y-BOCS (no OCD 71% improvement @ pre- or post-op) 6 mo 2. HDRS (82% significant worsening improvement @ 6 mo) @ 2 yr when IPG bat- 3. HARS (75% tery died improvement @ 6 mo)

1. YGTSS 50% mean reduction @ 3 mo

Tic Outcome Measures

Target: Thalamic

TABLE 1. Continued

(Continued)

1. Lead extender revision due to post-auricular discomfort, possible IPG malfunction with revision to abdominal placement 2. Stimulation-induced side effects: hyperkinetic left arm movement, right foot cramping, flashing in eyes, restlessness; Left lead quite medial

Not reported

4. Acute deterioration in tics with transient stim OFF—only 70% of previous control after back ON 5. Weight gain (n 5 1) 1. One pt did not tolerate DBS and turned OFF after 3 mo because of somatic complaints 2. Hardware malfunction (lead fracture) in 3 pts (because of: SIB tic, MVA, unknown) 3. Lead infection requiring bilateral lead replacement (n 5 1) 4. Increased anxiety in 2 pts (1 transient, 1 persistent, & fluctuating) Not reported

Adverse Events Reported

Welter et al., CM-Pf 1 GPi 3; *1 previ- 2F (36, 30); 200871 (limbic) ously 1M (30) reported(43)

27 (M)

0

0

1

pvGPi 1 CMSpv-Voi (*only GPi activated)

Ackermans et al., 200627

0

42 (F)

1

20–60 mo

IV

Controlled, III double-blind, randomized crossover study 1 open long-term f/u

Case report (part of 2 pt series)

IV

pGPi: 23 Case series mo; GPi (part of 1 ALIC/ 36 pt cohort) NA

1 yr

Tic Outcome Measures

Comorbidity Outcome Measures

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

1. BDI Yes (1 cut self No 2. STAI with knife, 1 3. YBOCS punched self in 4. VAS of social head) integration 2 pts with “rescue” ALIC/NA leads had only mild improvement on these measures pt with simultaneous CMPfc, Voa 1 ALIC/NA did have significant improvement (45%, 39%, 61%, 35%, respectively) 1. YGTSS 1. Y-BOCS (26% Not reported No 14% improvement reduction with GPi; for this case @ 23 mo with pGPi 16% further after 41% further ALIC/NA) improvement after 2. STAI (23% improveALIC/NA (49% total) ment with GPI; 12% further after ALIC/NA) 3. BDI (5% improvement with GPi; 30% further after ALIC/NA) 4. VAS of social integration (15% improvement with GPi; 12% further after ALIC/NA) 1. Videotaped exam 1. PI-R for compulsive No No with tic frequency symptoms—noted to (tics/min) by 2 have “total resolution” blinded raters ; 93% reduction 1. YGTSS None reported Yes (eye No (cross-over period) mutilation, burning of a) GPi): skin) 65%-96% improvement b) CM-Pf

1. YGTSS 2 pts had modest reduction in tics (23%-34%) after initial CMPfc,Voa DBS but depression/OCD remained disabling 83% reduction in pt with simultaneous CM-Pfc, Voa 1 ALIC/NA

Target: Multiple Targets

Level of Evidence

IV

Study Design

19–44 mo Case series (part of 4 pt cohort)

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

Servello et al., pGPi 1 ALIC/ NA add-on 201063

Sample size (n)

0

Target

25–37 (2M, Servello et al., CM-Pfc, Voa 3; *Also 1 ALIC/NA 1F) 200962 reported62 (n 5 1); CM-Pfc, Voa 1 ALIC/NA add-on (n 5 2)

Study

Target: Thalamic

TABLE 1. Continued

(Continued)

1. Thalamic—decreased libido in 1 pt 2. GPi—lethargy (3–4 d); nausea & vertigo at higher settings (n 5 2); anxiety (n 5 1)

1. Reduced energy level 2. Brief dystonic jerk each time turned ON

1. Required “rescue” ALIC/NA leads because of social impairment and poor QOL despite reduction in tics with GPi DBS

1. None reported 2. ALIC/NA rescue leads were not very effective

Adverse Events Reported

40 (F)

48, 19 (2M)

1

2

ALIC/NA (*later revised to CM DBS)

Shields et al., 200867

36 (F)

1 (19)

0

0

18 mo

11 mo

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

1

Sample size (n)

CM-Pf 1 GPi (limbic)

Target

Houeto et al., 200542

Study

Level of Evidence

Case series

Case report

IV

IV

III Prospective double-blind randomized N 5 1 crossover trial

Study Design

Comorbidity Outcome Measures

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

1. YGTSS

Yes

30%-64% improvement c) GPi 1 CM-Pf 43%-76% improvement 2. YGTSS (long-term f/u) CM-Pf/GPi ON (n 5 2; 74%-82% improvement) GPi ON (n 5 1; mild improvement) 3. RVTRS 1. YGTSS 1. MADRS Yes (eye mutila- No CM-Pf: 64% 2. BAS (anxiety) tion, burning of reduction skin) 3. BIS (impulsivity) GPi: 65% reduction SUMMARY: “Sham” STIM: worse CM-Pf: mood & than baseline impulsivity improved: SIB CM-Pf 1 GPi: 34 resolved (60% reduction) GPi: mood & impulsivity 2. RVTRS worse than CM-Pf; SIB CM-Pf: 77% resolved reduction SHAM: little change of GPi: 54% reduction depression/anxiety “Sham” STIM: 15% CM-Pf 1 GPi: SIB reduction resolved CM-Pf 1 GPi: 77% reduction 1. YGTSS None reported Yes (head-snap- No 23% improvement ping tics, limb fractures, retinal detachment)

Tic Outcome Measures

Target: Thalamic

TABLE 1. Continued

(Continued)

1. Lead extension fracture due to residual headsnapping tics after ALIC/ NA DBS 2. Stimulation-induced altered mood and impulse control problems 1. 48yoM:

1. Weight loss (18 kg with CM-Pf, continued with GPi)—may have been related to withdrawal of neuroleptics 2. During SHAM stim: SIB, excoriations at cables

Adverse Events Reported

1

37 (F)

0

18 mo

ALIC/NA

0

Flaherty et al., 200540

26 (M)

30 mo

1

ALIC/NA

Kuhn et al., 200745

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

37–107 mo

Sample size (n)

1. Midline thalamic 1 pvGPi 2. amGPi 1 midline thalamic 1 GPipv

Target

Motlagh et al., 201353

Study

Case report

Case report

Study Design

19yo with 3 targets had no improvement 48yo had 72% improvement

Tic Outcome Measures

IV

IV

1. Y-BOCS (52% improvement) 2. GAF—significantly improved (7->41)

Yes (head-snap- No ping tics, limb fracture, retinal detachments)

Yes

No

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

1. Y-BOCS – 48yo had Yes (2 of 2; slamsignificant improvement ming forearm against head, (29-->8); 19yo had no OCB head-snapping 2. HDRS – both had wor- tics 1 cervical injury; poking sening of depression 3. HARS – no change left eye, left cheek biting)

Comorbidity Outcome Measures

1. YGTSS None reported 25% improvement\ 2. Patient tic logs 45% decrease in frequency and severity

1. YGTSS 41% improvement 2. mRVTRS 50% improvement

Other Targets: ALIC/NA, STN

Level of Evidence

Target: Thalamic

TABLE 1. Continued

(Continued)

1. High stim requirements (2 IPG replacements in 30 mo) 2. Temporary deterioration in symptoms with battery depletion 3 2 1. Stim-induced dysarthria, rhythmic jaw clenching 2. High-voltage stim in ventral contacts (near NA)—mild apathy and depression; dorsal contacts in body of capsule—agitated hypomania (hrs to days onset for mood effects)

2nd target added due to continued head-snapping tics GPi lead extender malfunction due to headsnapping tics thalamic and GPi leads now OFF 2. 19yoM: ICU hospitalization with sedation for worsening tics 2mo after amGPi placement to prevent eye injury 3 separate DBS surgeries for 3 total bilateral targets due to refractory tics; currently has only R pvGPi lead on and no improvement

Adverse Events Reported

1

1

ALIC/NA

STN

Burdick et al., 201032

MartinezTorres et al., 200951 Servello et al., 200962

38 (M)

33 (M)

38 (M)

31 (M)

10 mo

1 yr

30 mo

36 mo

28 mo

IV

IV

IV

IV

Level of Evidence

Case series (part IV of 4 pt cohort)

Case report

Case report

Case report

Case report

Study Design

Comorbidity Outcome Measures

Yes (retinal detachment, blindness)

No

1. YGTSS 79% improvement

1. Y-BOCS (54% No improvement) 2. BDI (9% improvement; not significant) 3. STAI (19% improvement; not significant) 4. 10-pt VAS of social integration (no change)

No

1. YGTSS 1. Y-BOCS (56% Yes (self-mutila- No reduction) tion; breaking 44% improvement 2. mRVTRS glass in hands) 58% improvements 1. YGTSS 1. Y-BOCS (no significant No Yes 15% worse in 1st 6 improvement) mo 2. mRVTRS Tics 20% worse @ 30 mo (5->6) 1. RVTRS 1. UPDRS (pt had PD; No No 97% improvement 57% improvement)

1. 15-min videotaped None reported exams with tic counts 80% improvement

Tic Outcome Measures

Postoperative SIB With Immedi- Lead Location ate Risk of Bodily Reported (AC-PC Harm (Yes/No) Coordinates)

None reported

Not reported

Not reported

3. IPG accidentally turned off several times—symptom worsening 4. Fractured lead extension requiring replacement—due to tics 1. IPG malfunction at 9 months due to RUE motor tics ! sx deterioration ! improvement after IPG replaced 1. Rapid IPG depletion—2 IPG replacements in 36 months

Adverse Events Reported

BAS, Brief Anxiety Scale; BIS, Barratt’s Impulsivity Scale; CM-Pfc, Voa, centromedian nucleus-parafascicular, and ventro-oralis complex; CM-Spv-Voi, centromedian nucleus-substantia periventricularis-nucleus ventro-oralis internus complex; CM-Pf, centromedian nucleus–parafascicular complex; Vop-Voa-Voi 5 nucleus ventro-oralis posterior, ventro-oralis anterior, and ventro-oralis internus complex; Pf-DM-LM, parafascicular, dorsomedial nucleus, and lamella medialis; CM, centromedian nucleus region; GPi, globus pallidus internus; pvGPi, posteroventral globus pallidus internus; amGPi, anteromedial globus pallidus internus; YGTSS, Yale Global Tic Severity Rating Scale; Y-BOCS, YaleBrown Obsessive Compulsive Scale; BDI, Beck Depression Inventory; BDI-2, Beck Depression Inventory, 2nd Ed.; HARS, Hamilton Anxiety Rating Scale; HDRS, Hamilton Depression Rating Scale; STAI, State-Trait Anxiety Inventory; AC-PC, anterior commissure–posterior commissure; mRVTRS, modified Rush Video-based Tic Rating Scale; RVTRS, Rush Video-based Tic Rating Scale; CAARS, Conners Adult ADHD Rating Scale; PDD-SQ, Pervasive Developmental Disorder-Self Questionnaire; TSSL, Tourette Syndrome Symptom List; YMRS, Young Mania Rating Scale; QOLAS 5 Quality of Life Assessment Schedule; SRSI-90-R, Self-report symptom inventory 90 Items—revised; TSSR 5 Tic Symptom Self Report; BASC-2, Behavior Assessment System for Children—2nd Ed; TSGS, Tourette Syndrome Global Scale; PI-R, 5 Padua Inventory of obsessive compulsive disorder symptoms—Revised.

0

0

0

0

0

Age at DBS Subjects < 25 (years) yrs (ages) Follow-up

1;*Previously 47 (M) reported(64)

1

ALIC/NA

Neuner et al., 200954

ALIC/NA

1

Sample size (n)

ALIC/NA (unilateral R)

Target

Zabek et al., 200872

Study

Target: Thalamic

TABLE 1. Continued

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TABLE 2. Updates to 2006 TS DBS Guidelines 2006 Guidelines

Revised Guidelines

Diagnosis Agea

DSM-IV diagnosis of TS by expert clinician 25 yrs

Tic severity

1.Severe tic disorder with functional impairment 2. YGTSS > 35/50 3. Document with standardized video assessment 1. Tics should be the major symptom causing disability 2. Comorbid conditions should be stably treated 3. Comorbid conditions should be assessed using valid rating scales when available 1. Failed treatment trials from 3 pharmacological classes: a) alpha-adrenergic agonist, b) 2 dopamine agonists (typical & atypical), c) benzodiazepine 2. Evaluated for suitability of behavioral interventions for tics Stable for 6 months before DBS 1. Adequate social support without acute or subacute psychosocial stressors 2. Active involvement with psychological interventions when necessary

Neuropsychiatric comorbidities (ie, ADHD, OCB, depression, anxiety, etc.)

Failed conventional therapya

Comorbid medical disorders Psychosocial factors a

Suicidal/homicidal ideation (SI/HI)

a

Not specifically addressed

DSM-V diagnosis of TS by expert clinician 1. Age is not a strict criterion 2. Local ethics committee involvement for cases < 18 years old 1. Severe tic disorder with functional impairment 2. YGTSS > 35/50 3. Document with standardized video assessment 1. Tics should be the major symptom causing disability 2. Comorbid conditions should be stably treated 3. Comorbid conditions should be assessed using valid rating scales when available 1. Failed treatment trials from 3 pharmacological classes: a) alpha-adrenergic agonist, b) 2 dopamine agonists (typical & atypical), c) a drug from at least one additional class (eg, clonazepam, tetrabenazine) 2. A trial of CBIT should be offered Stable for 6 months before DBS 1. Adequate social support without acute or subacute psychosocial stressors 2. Active involvement with psychological interventions when necessary 3. Caregiver available to accompany patient for frequent follow-up 4. Psychogenic tics, embellishment, factitious symptoms, personality disorders, and malingering must be recognized and addressed Documentation of no active SI/HI for 6 months

a Recommendations have changed since 2006. TS, Tourette syndrome; DBS, deep brain stimulation; DSM, Diagnostic and Statistical Manual of Mental Disorders; YGTSS, Yale Global Tic Severity Scale; ADHD, attention deficit hyperactivity disorder; OCB, obsessive compulsive behaviors; CBIT, cognitive behavioral intervention therapy.

develop recommendations, and these were published in 2006.7 Subsequently, a collaborative international network of investigators was established, and in 2010 to 2011 the TSA commissioned an International Database/Registry of DBS outcomes and cases performed in patients with a diagnosis of TS. The purpose of this paper is to critically review the literature of all published cases of TS DBS and to provide updated opinions and recommendations for patient selection and assessment since 2006.7 Additionally, we aimed to encourage all clinicians and investigators who care for TS DBS patients to participate in the TSA DBS Database/Registry to collect more data and to enhance the understanding of surgical approaches and outcomes. Since 1999, 48 TS DBS studies have been published, including approximately 120 patients from 23 centers in 13 countries. At least seven separate brain targets have been employed27-72 (Table 1). The most commonly used targets have been the medial thalamic region targets (eg, centromedian nucleus–parafascicular complex [CM-Pf]), with 70 reported cases. Thirtyone cases of pallidal TS DBS have been reported and have included both anteromedial globus pallidus internus (GPi; “limbic”) targets (n 5 14) and posteroven-

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tral GPi targets (n 5 16). One case report of globus pallidus externa (GPe) DBS has also been published. The anterior limb of the internal capsule/nucleus accumbens target in isolation has been used in six case reports, and one case of STN DBS has been reported in a patient who had both tics and Parkinson’s disease. Eleven reported cases have employed more than one brain target (2 targets in 10 cases, and 1 case with 3 brain targets). In most of these cases, however, the additional target leads were added as “rescue” leads because of inadequate response to the initial TS DBS leads. Three cases reported were part of a prospective, double-blind, randomized crossover study comparing the CM-Pf and the anteromedial GPi targets.42,71 Although nearly all studies reported a beneficial effect on tics, most of these reports were uncontrolled cases (n 5 100), and the results revealed wide variations in study methods and outcomes, thus limiting meaningful interpretation. Approximately one fifth of the papers did not report using a validated outcome or videotape analysis. Rating scales to capture TS comorbidities (eg, obsessive-compulsive behavior, anxiety) were used in fewer than one third of reported

T O U R E T T E

studies, and postoperative DBS lead locations were reported in only 10 of 50 studies. Based on the levels of evidence classification scheme that has been used by the American Academy of Neurology,73 only four of these 48 studies30,49,55,71 met criteria for class III level of evidence (n 5 19), whereas the others were class IV. Given the small number of patients and the use of multiple brain targets within the class III studies, these data would likely receive the lowest evidence rating (level U), indicating that the therapy remains unproven because of inadequate or conflicting data. Since the last TSA guidelines were published in 2006,7 the field has gained important insight about safety and the potential for specific adverse effects of TS DBS. Thirty-three patients had TS DBS before the age of 25 years, including nine patients younger than 18. The risk of surgical complications and adverse events did not appear to be higher in these age groups when compared with patients older than 25 years. However, Servello et al.,61 in their series of 18 patients who underwent bilateral CM-Pf DBS, cautioned that three of the four cases who were implanted before the age of 20 years had less than satisfactory results after 3 to 6 months of follow-up (significant spontaneous waxing and waning of symptoms requiring frequent DBS programming). Ackermans et al.30 reported substantial improvement in six patients on the Yale Global Tic Severity Scale (YGTSS) between the ON and OFF stimulation conditions (37%), and also improvement after 6 months of open-label therapy (49%) in a double-blind randomized cross-over trial of centromedian nucleus– substantia periventricularis–nucleus ventro-oralis internus (CM-Spv-Vo) DBS. Significant adverse effects were reported, including decreased energy levels as well as subjective gaze disturbances. One patient with comorbid depression, pervasive developmental disorder, compulsions, and severe self-injurious behavior (SIB) had surgery under the condition of clinical urgency and had to be withdrawn from the trial because of severe postoperative complications with psychogenic paroxysmal hypertonia, disturbances of consciousness, and mutism. Somatoform disorder in this patient was only recognized retrospectively, and the patient eventually died of dehydration after refusing intravenous fluids.39 Servello et al.64 has reported the most robust experience with TS DBS, and also published an important paper analyzing the rates of infectious and hardwarerelated complications for different DBS indications (eg, PD, TS, tremor, and dystonia). Servello’s group reported an increased risk of infectious complications in TS DBS (7 of 39 [18%] patients) compared with an overall infection rate for all DBS indications of 3.7% (10 of 272 patients). The TS DBS patients also may be

S Y N D R O M E

D B S

G U I D E L I N E S

at increased risk for hardware malfunction. Six cases of lead or lead extension fractures, or alternatively IPG malfunction, have been reported,33,40,53,67,72 four of which were attributed to residual head-snapping tics. These findings highlight the unique and potentially severe issues in the TS population. Whereas tics that are life threatening or carry significant risk of immediate bodily harm are observed in only 5.1% of all TS patients, nearly 50 TS DBS cases with significant SIB have been reported in the literature, with more than half of these cases involving a severe behavior or risk of severe bodily harm (eg, cervical myelopathy from head-snapping tics, bone fractures, retinal detachment). Although few data are available to guide postoperative management of TS DBS patients, Servello et al. have the greatest experience with TS DBS to date. These authors have reported that TS DBS patients require more frequent visits for DBS adjustments (ie, in excess of monthly visits stipulated in their protocol) than for other DBS indications, and also TS DBS patients require substantial personal and family support. For this reason, a thorough evaluation of the patient’s adherence to recommendations, a clear assessment of the patient’s psychosocial situation inclusive of family dynamics, and the need for realistic patient and family expectations should be emphasized.58,61,63 Given the dearth of double-blind controlled studies of TS DBS, the lack of consistent outcome measures related to TS comorbidities, and the lack of rigorous studies comparing brain targets, few data are available to guide target choice either in general or in specific patients. Chronic continuous stimulation has been widely assumed to be the only effective approach to TS DBS. Recently, however, this notion has been challenged by Okun et al.,55 who demonstrated the potential of noncontinuous DBS paradigms in TS in a class III clinical trial planning study (n 5 5) of safety and preliminary effectiveness.55 Additionally, these authors have suggested that responsive approaches may be possible, especially by using oscillations (eg, the gamma band) and other brain network oscillations associated with DBS efficacy.74

Special Considerations Relevant to TS DBS and Guideline Updates The official DSM V diagnostic criteria require the presence of tics for more than a year, with onset before the age of 18 years, and occurrence of both multiple motor and at least one phonic tic for a definitive diagnosis of TS.1 The variability (variability of tic types, as well as the waxing and waning of tic severity) in TS provides an extra level of complexity when

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considering TS candidates for DBS therapy. Tics can be influenced by both environmental and psychological factors. Many TS patients can suppress tics partially or even completely for short periods, such as when being examined or when in public, but then release tics when returning to a more comfortable setting. The recognition of embellishment, psychogenic tics, factitious symptoms, personality disorders, and malingering all need to be considered in the preoperative workup,39,75-77 similar to the experience in epilepsy surgery with nonepileptic events.78 A clinician with expertise and experience with TS patients should confirm the diagnosis by strict criteria1 and address all psychological comorbidities and nonmotor features before consideration of DBS. Patientor family-expressed psychological “urgency” should not heavily influence the clinician’s decision to proceed to an operation.79,80 All psychological and non-motor features should be stabilized before consideration for surgery. The evaluating team should be aware that the usual onset of TS occurs before the age of 10 years and has an average onset of 5.6 years. Tics typically follow a waxing and waning course, and they peak in severity in early adolescence. This peak is followed in most cases by a gradual reduction in tic severity in late adolescence and early adulthood.6,81 Longitudinal studies have reported either complete remission or alternatively mild tics in early adulthood for more than two thirds of TS patients.5,6 Clinicians selecting DBS candidates would likely benefit from a list of predictive factors that would facilitate identification of patients who will remain severely affected into adulthood. This information is not currently known. Recent research suggests that tic severity, premonitory urges, and a family history of TS may be childhood predictors of a worse health-related quality of life in adulthood.82 Although TS rarely causes severe disability, and generally has a favorable prognosis, in a small subset of patients the symptoms cause severe disruption of interpersonal relationships, as well as impairments of social, psychological, and intellectual development. In extreme cases, TS may even become life threatening (eg, whiplash tics causing vertebral artery dissection83 or myelopathy84). This severe form of the syndrome is associated with a higher rate of behavioral comorbidities (particularly OCD) and is more likely to be refractory to conservative medical management. Although malignant TS may affect only 5.1% of all TS patients, these cases will frequently come to the attention of TS DBS teams.85 The appropriate age to perform TS DBS is unknown and has been widely debated. In 2006, the first TSA guidelines7 proposed a minimum age criterion of 25 years to ensure that individuals who might experience spontaneous tic remission would not be implanted with a surgical device. Since that time,

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compelling arguments have been made for consideration of surgical intervention at younger ages in certain cases of severe TS.86,87 The risk–benefit data for TS and for other DBS indications have shown that the actual DBS procedure is safe and well tolerated in children, particularly as demonstrated in those with dystonia.88 Because of increased evidence of a favorable risk–benefit ratio for DBS in children with dystonia and TS, the age guideline has been adjusted by most experts to recommend a multidisciplinary evaluation and discussion, without setting a firm age limit. Delaying surgery in younger incapacitated TS patients could potentially result in irreparable harm to social, psychological, and intellectual development, even if the symptoms eventually subside with age. Similarly, in rare cases of “malignant tics” that occur in younger individuals, the tics themselves (eg, whiplash tics) may carry greater risk for bodily harm, paralysis, or even death. A feature of TS with implications for determining the efficacy of DBS is its frequent association with disabling psychiatric and behavioral comorbidities. The most common of these are ADHD and OCD. Comorbidities have a significant negative impact on the quality of life in TS and can be a larger source of impairment when compared with motor tics.89,90 Identification of comorbid psychiatric symptoms is critical for a DBS workup, because when left untreated, these symptoms may be the best predictors of a worse quality of life, with or without DBS therapy.91 Comorbid symptoms should be adequately treated before surgery, and patients should be informed that individuals who are deemed to be good candidates for DBS may experience a 30% to 50% or greater improvement in motor tics. However, based on all available published cases, how DBS will impact TS comorbidities remains unclear. Notably, comorbid OCD, ADHD, and mood issues have improved after DBS in some but not all cases.31,33,36,45,52,54,57,58,63,65,66 Deep brain stimulation should be offered to TS patients only after evaluation by a multidisciplinary or interdisciplinary team. This team should include experts in TS and associated comorbidities (ie, neurologist, neurosurgeon, psychiatrist, neuropsychologist, DBS programmer [nurse or physician]). Centers performing DBS should have a high level of expertise with DBS therapy, especially given the complexities of the TS patient. Potential therapy candidates should be independently evaluated by each member of the team, and discussion of candidacy, risks, benefits, operative approach, and postoperative care should be pursued before a decision on candidacy is reached. The ideal DBS candidate will have a DSM V diagnosis of TS and severe motor and vocal tics, which despite exhaustive medical and behavioral treatment trials result in significant impairment of self-esteem,

T O U R E T T E

TABLE 3. Pre- and post-operative outcome measures recommended by the TSA* Preoperative Information: Patient Assessment and Selection Age, sex, ethnicity Age of TS onset Age at diagnosis of TS Age at time of surgery Psychiatric comorbidities (OCB, ADHD, depression, anxiety, SIB, other) TS medications tried and stopped bfore DBS (medication name, dose, and duration of trial) TS medications at the time of DBS (including dose) Documentation of CBIT being offered or of the trial and outcome Standardized evaluation of tic type and severity (pre- and postoperatively) Yale Global Tic Severity Score (YGTSS) Blinded video-based rating (e.g., Rush video scale rating of body regions involved, tic severity and frequency) Premonitory Urge for Tics Scale 132 Clinical Global Impression (CGI for TS) Standardized evaluation of comorbid symptoms with valid and reliable instruments when available (pre- and post-operatively) Yale-Brown Obsessive Compulsive Scale (Y-BOCS) Conners’ Adult ADHD Rating Scale (CAARS) Depression: Beck Depression Inventory, 2nd Ed. (BDI-2), Hamilton Depression Rating Scale (HDRS), Montgomery-Asberg Depression Rating Scale (MADRS) Anxiety: Hamilton Anxiety Rating Scale (HARS), State-Trait Anxiety Inventory (STAI) Mania: Young Mania Rating Scale (YMRS), K-SADS Mania Rating Scale (MRS) CGI (for ADHD and OCD) Suicide Assessment Scale (e.g., Columbia Suicide Severity Rating Scale) Quality of Life Measurement (eg, Gilles-de-la-Tourette-Syndrome Quality-of-Life scale [GTS-QOL], Global Assessment of Functioning scale [GAF], SF-36) Surgical information: targeting and lead location Brain target (eg, CM-Pfc-Voa thalamus, Gpi, ALIC/NA, other) Procedure (unilateral, bilateral, simultaneous, staged) Lead models and IPG models used (eg, Medtronic 3387/3389, ANS, Neuropace, primary cell, rechargeable, other) Lead location verification with postoperative MRI or CT (x-y-z coordinates of each contact in relation to the midcommissural point) Postoperative information: programming, outcome data and adverse events Stimulation parameters (active contacts, amplitude or current, frequency, pulse width, 6 impedence) at each follow-up visit and time duration at that setting Frequency of programming adjustments (# to optimization, # per year) Stimulation-induced and general adverse effects Psychiatric/cognitive (exacerbation of tics, mania, hypomania, cognitive decline, anxiety, OCB, depression, smile or laughter induction, impulsivity, psychosis, suicidal ideation/attempt, completed suicide, other) General (paresthesias, muscle contractions, dyskinesias, bradykinesia, dystonia, dysarthria, stuttering, nausea or vertigo, lethargy, gait disorder, sexual side effects, weight loss/gain >10 pounds, death, other) Intraoperative or early surgical (1st post-op week) adverse events (symptomatic/asymptomatic hemorrhage, ischemic stroke, seizure, postop confusion, infection, air embolism, DVT, death, other) Delayed surgical adverse events (infection of intracranial lead, extracranial lead/lead extender infection, infection of IPG, lead dislodgment, lead fracture, lead revision, suboptimally positioned lead, lead removal, IPG removal, other) Timing of IPG replacement or need for recharging (Continued)

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D B S

G U I D E L I N E S

Regular postoperative evaluations to include standardized rating scales of TS and co-morbidities YGTSS Blinded video-based rating Y-BOCS Premonitory Urge for Tics Scale (PUTS) 132 Conner’s ADHD Scale Depression: BDI-2, HDRS or MADRS Anxiety: HARS, STAI Mania: YMRS, K-SADS, MRS CGI Suicide Assessment Scale (eg, Columbia Suicide Severity Rating Scale) a

The exact measures are less important than the adherence to measurement of pre/post outcomes in each of the major domains (motor, nonmotor, mood, quality of life). TSA, Tourette Syndrome Association; TS, Tourette syndrome; OCB, obsessive compulsive behaviors; ADHD, attention deficit hyperactivity disorder; SIB, self-injurious behavior; DBS, deep brain stimulation; CBIT, cognitive behavioral intervention therapy; K-SADS, kiddie schedule for affective disorders and schizophrenia; OCD, obsessive-compulsive disorder; SF-36, short form health surgery 36; CM-Pfc-Voa, centromedian nucleus-parafascicular complex; Gpi, globus pallipus internus; ALIC/NA, anterior limb of the internal capsule/nucleus accumbens; IPG, implantable—pulse generator; MRI, magnetic resonance imaging; CT, computed tomography; DVT, deep venus thrombosis.

social acceptance, family life, school or job functioning, or physical well-being. Psychosocial, medical, neurological, or psychiatric conditions that increase the risk of the procedure, preclude full participation in the operation or post-DBS care, or that will potentially compromise the accurate assessment of outcomes should all be addressed by the DBS multidisciplinary team before surgery. Tics and comorbid conditions should be optimally treated medically and behaviorally per current expert standards.3,9 Deep brain stimulation should not be performed during periods of severe psychosocial instability, which is likely to interfere with the close monitoring and follow-up required. Psychosocial stress also may increase the risk of suicide after surgery.92,93 In general, DBS surgery should be avoided if a patient is judged to be at imminent risk of suicide.80

Inclusion and Exclusion Criteria A DSM V diagnosis of TS should be made by an expert clinician who has experience in the evaluation and management of tic disorders (updated from DSM IV). Age should no longer be a strict criterion. Deep brain stimulation should be considered only when all standard medical and behavioral therapies have failed regardless of the patient’s age. Tourette syndrome DBS should rarely be an urgent indication, with the possible exception of impending paralysis from headsnapping tics or profound SIB. A local ethics committee or institutional review board should be consulted for consideration of cases involving persons younger than 18 years of age, as well as in cases with urgent indications, particularly those with lower YGTSS scores or with shorter durations of symptoms.

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TABLE 4. TS DBS Inclusion and Exclusion Criteria Inclusion Criteria

1. DSM-V Diagnosis of TS by expert clinician 2. Age is not a strict criterion. Local ethics committee involvement for cases involving persons < 18 years, and for cases considered “urgent” (eg, impending paralysis from headsnapping tics) 3. Tic Severity: YGTSS >35/50 4. Tics are primary cause of disability 5. Tics are refractory to conservative therapy (failed trials of medications from 3 classes, CBIT offered) 6. Co-morbid medical, neurological, and psychiatric disorders are treated and stable 3 6 months 7. Psychosocial environment is stable 8. Demonstrated ability to adhere to recommended treatments 9. Neuropsychological profile indicates candidate can tolerate demands of surgery, postoperative follow-up, and possibility of poor outcome

Exclusion Criteria

1. Active suicidal or homicidal ideation within 6 months 2. Active or recent substance abuse 3. Structural lesions on brain MRI 4. Medical, neurological, or psychiatric disorders that increase the risk of a failed procedure or interference with postoperative management 5. Malingering, factitious disorder, or psychogenic tics

TS, Tourette syndrome; DBS, deep brain stimulation; DSM-V, Diagnostic and Statistical Manual of Mental Disorders; YGTSS, Yale Global Tic Severity Scale; CBIT, cognitive behavioral intervention therapy.

The candidate should have a chronic and severe tic disorder with severe functional impairment. A standardized videotape assessment (eg, Rush Video-Based Tic Rating Scale94) and a validated rating scale (eg, Yale Global Tic Severity Scale [YGTSS]95) should be used to document tic severity. In most cases the TS patient should have a total YGTSS score greater than 35/50 documented over the course of a year. Motor or vocal tics should be the primary symptom causing disability for a patient. Although most candidates are likely to have comorbid ADHD, OCD, depression, anxiety, or other non-motor symptoms, these symptoms should be adequately treated and stable for a minimum of 6 months and should not be the major source of functional impairment. In some patients, the commonly noted comorbidity of SIB, particularly severe SIB,96 may be inextricably intertwined with tics, and thus may be a primary contributor to disability. Patients with SIB or picking behavior should be warned preoperatively of an increased risk of infection or hardware-related complications.64 At a minimum, documentation of unsuccessful treatment trials is needed from three pharmacological classes: (1) an alpha-adrenergic agonist, (2) two dopamine antagonists (including one typical and one atypical), and (3) a drug from at least one additional class (e.g., clonazepam, topiramate, or tetrabenazine). Tet-

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rabenazine should be tried if accessible.97,98 In addition, CBIT delivered by a trained CBIT therapist should be offered,2,4 and the patient must have demonstrated his or her ability to adhere to recommended treatment plans before serious surgical consideration. Unfortunately, in many locations, including some centers experienced with TS, substantial issues of access, wait times, and lack of insurance reimbursement make therapies such as CBIT not always feasible, particularly in cases of malignant TS. The neuropsychological profile must indicate that the candidate will be well suited to tolerate the surgical procedure, rigorous postoperative follow-up, and the possibility of both a negative or positive outcome.87 The potential for progressive cognitive impairment should be absent on this profile, or a follow-up profile should be performed to confirm findings and to also track progression. Because of the substantial time commitment required for optimization of DBS therapy, as well as the significant impact that psychosocial factors can have on the disorder, any candidate for TS DBS must have adequate social support, and there should not be acute or subacute psychosocial stressors. A caregiver must be available to accompany the patient for visits and for frequent programming. Similar to that proposed in the previous guidelines, there should be documentation of no suicidal ideation and no psychiatric hospitalization for 6 months before surgery. Depression and mood disorders must be stable and treated. Preferably suicidal tendency should be monitored preoperatively and postoperatively with a scale such as the Columbia Suicide Scale99 or another similar measure. Active or recent dependence on drugs or alcohol are contraindications for surgery. No structural lesions should be seen on magnetic resonance imaging that are deemed to present a significant risk by the neurosurgeon, nor medical, neurological, or cognitive disorders that would significantly increase the risk of a failed procedure, surgical complications, or interfere with postoperative management. A new criterion employed by most centers involved with TS DBS since 2006 is that an expert clinician should feel comfortable that malingering, factitious disorder, or psychogenic tics are not present. Teams implanting TS patients should record preoperative and postoperative outcome measures, including age, disease duration, tic subtypes, motor, mood, behavior, quality of life, medications, postoperative lead locations, stimulation settings, and suicidal tendencies. Validated clinical rating scales of tics and TS comorbidities are critical. A full list of the measures recommended by the TSA and employed in in the International TSA DBS Database/Registry is provided in Table 3. The exact measures are less important than the adherence to measurement of preoperative

T O U R E T T E

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D B S

G U I D E L I N E S

FIG. 1. Flow diagram of recommended DBS evaluation process for TS.

and postoperative outcomes in each of the major domains (motor, non-motor, mood, quality of life).

Discussion The centers participating in the TSA International Database/Registry have employed several important practice pattern changes to the selection and assessment recommendations for the use of TS DBS. These

changes were based on the expanded experience in the field since the 2006 guidelines. The changes and particularly the inclusion criteria (Table 4) reflect the growing experience with more than 120 cases reported worldwide. In particular, the relative safety of the procedure has been better established. Additionally, some TS cases may be appropriate for DBS before the previously recommended age of 25 years. Most centers now employ a multidisciplinary team approach for screening rather than an age limit. For patients younger than age

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18, one should have additional institutional approval. Centers performing TS DBS should use preoperative and postoperative outcome measures, regardless of whether they adopt the TS DBS Database/Registry guidelines. All patients undergoing TS DBS should be aware that there is a reasonable chance for motor and vocal tic improvement, but that other co-morbidities in general respond less consistently to therapy. Clinicians should educate patients and families on the increased infection rate, and the potential for increased hardware-related issues. Figure 1 provides a diagram of the recommended evaluation before TS DBS. The most appropriate brain target for an individual symptom profile remains unknown. The consensus of the centers implanting TS DBS includes the following: (1) all adverse events, whether major or minor, surgical or nonsurgical, related or unrelated to the therapy, should be recorded and reported; (2) detailed descriptions of all surgical and programming procedures should be recorded; and (3) preoperative and postoperative targeting should be reported, because where the optimal target regions are located, even within targets, remains unclear. Psychological issues should be screened preoperatively and monitored postoperatively. Finally, rigorous reporting of DBS failures and adverse events is needed.100 Databases and registries may be our best hope of advancing the field quickly, because most expert centers will do less than a handful of TS surgeries. After an extensive review of the literature and consensus among implanters of DBS, we conclude that TS DBS, though still evolving, is a promising approach for a subset of medication-refractory and severely affected patients.

10.

Kleiner-Fisman G, Herzog J, Fisman DN, et al. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord 2006;21(Suppl 14):S290-S304.

11.

Pahwa R, Factor SA, Lyons KE, et al. Practice parameter: treatment of Parkinson disease with motor fluctuations and dyskinesia (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2006;66:983-995.

12.

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.

13.

Lyons KE, Pahwa R. Deep brain stimulation and tremor. Neurotherapeutics 2008;5:331-338.

14.

Zesiewicz TA, Elble R, Louis ED, et al. Practice parameter: therapies for essential tremor: report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2005; 64:2008-2020.

15.

Kupsch A, Benecke R, Muller J, et al. Pallidal deep-brain stimulation in primary generalized or segmental dystonia. N Engl J Med 2006;355:1978-1990.

16.

Ostrem JL, Starr PA. Treatment of dystonia with deep brain stimulation. Neurotherapeutics 2008;5:320-330.

17.

Vidailhet M, Vercueil L, Houeto JL, et al. Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. N Engl J Med 2005;352:459-467.

18.

Greenberg BD, Malone DA, Friehs GM, et al. Three-year outcomes in deep brain stimulation for highly resistant obsessive-compulsive disorder. Neuropsychopharmacology 2006;31:2384-2393.

19.

Greenberg BD, Gabriels LA, Malone DAJ, et al. Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessivecompulsive disorder: worldwide experience. Mol Psychiatry 2010; 15:64-79.

20.

Bronstein JM, Tagliati M, Alterman RL, et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol 2011;68:165.

21.

Bronte-Stewart H, Taira T, Valldeoriola F, et al. Inclusion and exclusion criteria for DBS in dystonia. Mov Disord 2011;26(Suppl 1):S5-S16.

22.

Greenberg BD, Price LH, Rauch SL, et al. Neurosurgery for intractable obsessive-compulsive disorder and depression: critical issues. Neurosurg Clin North Am 2003;14:199-212.

23.

Cavanna AE, Eddy CM, Mitchell R, et al. An approach to deep brain stimulation for severe treatment-refractory Tourette syndrome: the UK perspective. Br J Neurosurg 2011;25:38-44.

24.

Muller-Vahl KR, Cath DC, Cavanna AE, et al. European clinical guidelines for Tourette syndrome and other tic disorders. Part IV: deep brain stimulation. Eur Child Adolesc Psychiatry 2011;20:209-217.

25.

Farris S, Giroux M. Retrospective review of factors leading to dissatisfaction with subthalamic nucleus deep brain stimulation during long-term management. Surg Neurol Int 2013;4:69.

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Tourette syndrome deep brain stimulation: a review and updated recommendations.

Deep brain stimulation (DBS) may improve disabling tics in severely affected medication and behaviorally resistant Tourette syndrome (TS). Here we rev...
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