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1 Supplementary Appendix This appendix has been provided by the authors to give readers additional information about their work. Supplement to: Elias WJ, Lipsman N, Ondo WG, et al. A randomized trial of focused ultrasound thalamotomy for essential tremor. N Engl J Med 2016;375: DOI: /NEJMoa
2 SUPPLEMENTAL APPENDIX A Randomized Trial of Focused Ultrasound Thalamotomy for Essential Tremor W. Jeffrey Elias MD 1, Nir Lipsman MD PhD 2, William G. Ondo MD 3, Pejman Ghanouni MD PhD 4, Young Goo Kim MD PhD 5, Wonhee Lee MD PhD 5, Michael Schwartz MD MSc 6, Kullervo Hynynen PhD 6, Andres M. Lozano MD 2, Binit B. Shah MD 1, Diane Huss DPT NCS 1, Robert F. Dallapiazza MD PhD 1, Ryder Gwinn MD 7, Jennifer Witt MD 7, Susie Ro MD 7, Howard M. Eisenberg MD PhD 8, Paul S. Fishman MD PhD 8, Dheeraj Gandhi MD MBBS 8, Casey H. Halpern MD 4, Rosalind Chuang MD 7, Kim Butts Pauly PhD 4, Travis S. Tierney MD PhD 9, Michael T. Hayes MD 10, G. Rees Cosgrove MD 10, Toshio Yamaguchi MD PhD 11, Keiichi Abe MD 11, Takaomi Taira MD PhD 11, and Jin Woo Chang MD PhD 5 1 University of Virginia Health Sciences Center, Charlottesville, Virginia 2 Toronto Western Hospital, Toronto, Canada 3 Methodist Neurological Institute, Houston, Texas 4 Stanford University School of Medicine, Stanford, California 5 Yonsei University College of Medicine, Seoul, Korea 6 Sunnybrook Health Sciences Center, Toronto, Canada 7 Swedish Neuroscience Institute, Seattle, Washington 8 University of Maryland School of Medicine, Baltimore, Maryland 9 University of Miami School of Medicine, Nicklaus Children s Hospital, Miami, Florida 10 Brigham and Women s Hospital, Boston, Massachusetts 11 Tokyo Women s Medical University, Tokyo, Japan 1
3 Table of Contents Figure S1. Transcranial MR guided focused ultrasound 3 Focused ultrasound thalamotomy procedure 4 Figure S2. Study design and patient accountability 5 Sensitivity analysis for screen failures following randomization 6 Table S1. Tremor scores, upper limb 8 Figure S3. Tremor scores, upper limb (unblinded cohort) 8 Table S2. Tremor scores, total 9 Figure S4. Tremor scores, total 9 Table S3. Functional activities of daily life from Part C of Clinical Rating Scale 10 Table S4. Quality of Life scores from QUEST 11 Table S5. Adverse events: unblinded treatments (N=21) [open-label, extension phase + retreatments] 12 Table S6. Unrelated adverse events 13 Publication committee 14 Data Safety Monitoring Board 14 Study dates 14 2
4 Figure S1: Transcranial MRI guided focused ultrasound. (A) The system couples a multi-element, phased-array, ultrasound transducer with 3 Tesla MRI. (B) Each of the 1,024 elements operates at 650 khz and can be individually controlled to focus acoustic energy through the intact skull to a single target. Stereotactic MRI planning simulates the acoustic beam path to the target. (C) MRI thermometry measures temperature change with 1⁰ Celsius resolution, so that the intensity and location of the acoustic focus and surrounding brain is carefully and continuously monitored. (D) Precise stereotactic focused ultrasound thalamotomy is achieved with thermal ablation through the intact skull. 3
5 Focused ultrasound thalamotomy procedure Patients presented on the morning of the procedure without taking their tremor medications and were prepared with hair shaving, placement of a stereotactic head frame under local anesthesia, and intravenous access. A rubber membrane was affixed to the scalp and coupled to the MRI-compatible ultrasound transducer so that chilled and degassed water could be circulated around the scalp. Patients were then positioned into the bore of the magnet for the procedure. They were awake and responsive to allow for intra-procedural clinical monitoring. MRI was acquired so that the ventralis intermedius thalamic target could be planned in relation to the anterior and posterior commissures, a standard stereotactic reference line. Preoperative CT and MRI were fused to the procedural MRI obtained with the head in the frame and water bath. No pass regions were designated for the acoustic energy path and included air sinuses, intracranial calcifications, and folds in the rubber membrane. For subjects in the treatment arm, acoustic energy was titrated in three phases while continuously monitoring the intensity and location of the ultrasound focus with MR thermometry. First the ultrasound focus was visualized by applying low energy sonications that resulted in a minimal thermal rise of 3-5 ⁰C. Next acoustic energy was sequentially escalated to observe for clinical response or neurologic effects with moderate heating (50-54⁰C), so that the target could be adjusted prior to permanent lesioning. Finally, thalamic ablation was prescribed with peak voxel temperatures reaching Celsius, and it could be repeated if tremor persisted. At the completion of the procedure, the frame was removed and the patients recovered in the hospital overnight. Neurologic examination and postoperative MRI were obtained before discharge. 4
6 Figure S2: Study design and accountability. There was high accountability in this randomized (3:1) trial with 97% reaching the primary endpoint assessment at 3 months and 88% completed the one year study period. * *Five subjects were excluded following randomization and before their procedures. The reasons for exclusion are listed below and a sensitivity analysis was performed. As predefined in the protocol and statistical analysis plan, the intent-to-treat analysis only included those patients (N=76) who attempted or completed a procedure. 5
7 Sensitivity Analysis for screen failures (N=5) following randomization There were 5 subjects who were excluded from the study following randomization but before their procedures for the following reasons: Unsuitable skull (identified by skull density ratio from CT); N=2 Patient withdrawal due to anxiety Vascular risk identified on MRI (missed on first interpretation) Investigator discretion It is important to evaluate both the Best and the Worst case scenario by imputing a best/worst case scenarios of the primary outcome measure for the 5 screen failure subjects: All 5 subjects were randomized to FUS thalamotomy, so both worse- and bestcase imputations were done in this group Worst-case: imputing the 10 th percentile improvement in the FUS thalamotomy is shown in the first table. Best-case: imputing the 90 th percentile improvement in the ExAblate group is shown in the second table. Worst-Case Imputation: percent improvement of upper limb CRST subscore from baseline to 3 months post treatment Treatment Group FUS Sham P-Value Mean <0.001 Std Min Median Max % Lower CL % Upper CL N T-test was applied for the comparison between treatment groups since the data did not differ appreciably from normal theory 2. PE was calculated as Percent Change ({(Baseline - Visit)/Baseline}*100) 3. Higher PE values represent improvement. 4. The presented confidence intervals are 95% intervals for the mean. 6
8 Best-Case Imputation: percent improvement of upper limb CRST subscore from baseline to 3 months post treatment Treatment Group PE FUS Sham P-Value Mean <0.001 Std Min Median Max % Lower CL % Upper CL N T-test was applied for the comparison between treatment groups since the data did not differ appreciably from normal theory 2. PE was calculated as Percent Change ({(Baseline - Visit)/Baseline}*100) 3. Higher PE values represent improvement Conclusion Neither best- nor worst-case imputations meaningfully influence the results. The mean improvement in the primary endpoint (% change in upper limb tremor at 3 months as compared to baseline) for FUS thalamotomy and sham are: Reported: 46.9% and -0.1% Worst Case: 44.2% and -0.1% Best Case: 49.2% and -0.1% There is a less than 3% difference in the scenarios from the reported results, and there is no impact on the p-value between cohorts nor with the 95% Confidence interval. Under all scenarios, FUS thalamotomy more effective improved the primary outcome measure than sham procedures at p <
9 Table S1. Tremor scores, upper limb Upper Limb Tremor (treated hand) Mean CRST Intent to Treat score (32 pts max) FUS (N=56) Sham (N=20) P value, Between groups P value, Within FUS Group Unblinded FUS: crossover (19) & Re-treat (2) (N=21) Baseline ± ± ± 4.21 Month ± ± 3.68 Not tested ± 4.06 Month ± ± ± 3.88 Month ± ± 3.86 Month ± ± 4.7* *N = 9 at 12 months Figure S3. Tremor scores, upper limb (unblinded cohort) Group results for upper limb tremor in 21 patients treated after the blinded phase. This group includes 19 sham crossovers and 2 prior thalamotomy who were re-treated after technical issues. Mean improvement from baseline was significant (p<0.001) at each post treatment timepoint. Bars indicate 95% CI. 8
10 Table S2. Tremor scores, total Overall Tremor Mean CRST score (152 pts max) FUS N=56 Intent to Treat Sham N=20 Unblinded FUS: crossover (19) & Re-treat (2) N=21 Baseline ± ± ± Month ± ± ± 9.60 Month ± ± ± Month ± ± Month ± ± 16.02* * N= 9 at 12 months Figure S4. Tremor scores, total Total tremor scores from the Clinical Rating Scale for Tremor statistically improved as compared to baseline following unilateral focused ultrasound thalamotomy. There was no improvement with sham procedures. 9
11 Table S3. Functional activities of daily life Functional Activities (Clinical Rating Scale for Tremor, Part C) Disabilities Baseline 3 months 12 months (0-4 pts each) FUS (N=56) Sham (N=20) FUS (N=54) Sham (N=20) FUS (N=51) Speaking 0.73 ± ± ± ± ± 0.97 Eating 2.38 ± ± ± ± ± 0.98 Drinking 2.98 ± ± ± ± ± 1.17 Hygiene 2.46 ± ± ± ± ± 1.10 Dressing 1.59 ± ± ± ± ± 0.85 Writing 2.63 ± ± ± ± ± 1.14 Working 2.21 ± ± ± ± ± 1.10 Social 1.55 ± ± ± ± ± 0.80 TOTAL * (32 pts max) ± ± ± ± ± 6.15 *Focused ultrasound thalamotomy significantly improved total disability score at 3 months in comparison to sham procedures. (p<0.001) 10
12 Table S4. Quality of life Quality of Life in Essential Tremor Questionnaire Domains Baseline 3 months 12 months FUS (N=56) Sham (N=20) FUS (N=54) Sham (N=20) FUS (N=51) Communication ± ± ± ± ± Work and Finances ± ± ± ± ± Hobbies and Leisure ± ± ± ± ± Physical Score ± ± ± ± ± Psychosocial ± ± ± ± ± Total* ± ± ± ± ± * Focused ultrasound thalamotomy significantly improved total quality of life score at 3 months in comparison to sham procedures. (p<0.001) 11
13 Table S5. Adverse events: unblinded treatments This third cohort represented 21 patients who underwent focused ultrasound thalamotomy in an unblinded fashion. 19 patients from the sham cohort elected for the treatment after the 3 month blinded period as part of an open-label, extension phase. Two patients from the treatment cohort were re-treated because of previous technical issues. (Figure S2) Adverse event Paresthesia / numbness: face, lips, tongue Focused Ultrasound Thalamotomy (N=21) Total # 1d 7d 1m 3m 6m 12m 6 (29) (24) hand, fingers 5 (24) (5) Taste disturbance 2 (10) (10) Gait disturbance: 3 (14) Ataxia (objectively noted on clinical exam) Gait disturbance: 5 (24) (5) unsteady, unbalanced (subjective report from examiner or patient) Dysmetria, limb 3 (14) (10) Contralateral weakness 3 (14) * (5) Dysarthria 3 (14) **(10) Headache 7 (33) 6 Fatigue 4 (19) (10) Dysequilibrium sensation 3 (14) (5) Intraprocedural sensations, events 1 Head pains 7 (33) ( heat, pressure ) Dizzy 4 (19) Nausea 3 (14) Vomit 1 (5) Vertigo 1 (5) Events attributed to placement of a stereotactic frame Pin site pain, edema, 7 (33) bruising Number of observed adverse events with ( ) indicating percentage. Numbers reported at each study visit represent the number of adverse events still present. Adverse events reported at 12 months are ongoing. 1 None of the procedures were interrupted or suspended. *physical therapy prescribed **speech therapy prescribed 12
14 Table S6. Unrelated adverse events Event Incidence TIA 1 1 Sick sinus syndrome 2 1 Hypertension 8 Bradycardia 2 Vertigo 2 Ankle pain 2 Myoclonus, hand 1 Memory loss 1 Hypotension 1 Urethral irritation 1 Erythema 1 Common cold 1 Ear infection 1 Nausea 1 Hypersalivation 1 Hiccups 1 Blurred vision 1 Prostatic hyperplasia 1 Hip pain 1 Urinary urgency 1 Impatience 1 Episodic dizziness 1 Scalp sores 1 Skin rash 1 Urticarial 1 Tearing 1 PVCs 1 Flu 1 Dry mouth 1 These events were deemed unrelated to the focused ultrasound thalamotomy or sham procedures. 1 TIA occurring in one of the patients 6 weeks following a thalamotomy procedure from the primary analysis. Resolved within 3 days and categorized as serious adverse event. 2 Sick sinus syndrome requiring hospitalization after a crossover treatment. 13
15 Publication committee: W. Jeffrey Elias MD (principal investigator), Jin Woo Chang MD PhD, Nir Lipsman MD PhD, Ryder Gwinn MD, Pejman Ghanouni MD PhD, Howard M. Eisenberg MD, Travis Tierney MD PhD, G. Rees Cosgrove MD, Takaomi Taira MD PhD, and William G. Ondo MD. Data Safety Monitoring Board: Robert G. Grossman MD, Houston Methodist Hospital L. Dade Lunsford MD, University of Pittsburgh Medical Center William G. Bradley, University of California at San Diego Study dates Study initiation: June 12, 2013 Study completion: September 15,
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