Background: Holmes tremor (HT) arises from disruption of the cerebellothalamocortical pathways. A lesion can interrupt the projection at any point, resulting in this tremor. We describe a case of HT due to the rare artery of Percheron infarct and its successful treatment using deep brain stimulation.

Case report: A 62-year-old woman with a right medial cerebral peduncle and bilateral thalamic stroke developed HT. Ventral intermediate nucleus (Vim) zona incerta (ZI) deep brain stimulation (DBS) surgery was performed, with improvement in her tremor.

Discussion: Our case supports the theory that the more caudal ZI target in combination with Vim is beneficial in treating poorly DBS-responsive tremors such as HT

Elkind, Mitchell S.

Ford, Blair

O'Shea, Sarah A.

Pullman, Seth L.

English

Columbia University Academic Commons

1Case ReportsHolmes Tremor due to Artery of Percheron Infarct:  Clinical Case and Treatment Using Deep Brain Stimulation  of the Vim and ZI TargetsSarah A. O’Shea1,2*, Mitchell Elkind2,3, Seth L. Pullman2 & Blair Ford21Department of Neurology, Boston University School of Medicine, Boston University, Boston, MA, USA,  2Department of Neurology, College of Physicians and Surgeons, Columbia University, New York, NY, USA,  3Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USAIntroductionHolmes tremor (HT) is characterized as a 3–4-Hz flexor-extension oscillation and was initially described by Gordon Holmes in 1904 as a tremor that is present at rest, then exacerbated with posture, and further intensified with movement.1 The etiologies of  HT vary, and are associ-ated with lesions involving the cerebellothalamic pathways. HT is fre-quently associated with vascular lesions, but may also result from demyelinating lesions, infectious diseases, malignancy, vascular malfor-mations, and traumatic brain injury (TBI).2,3 The localization also varies significantly, and lesions associated with HT are known to occur in the midbrain, pons, thalamus, and cerebellum.4 Cases of  HT and parkin-sonism involving vascular lesions secondary to the occlusion of  the artery of  Percheron (AOP) have also been reported6; however, successful treatment of  such a tremor secondary to this particular lesion with both the ventral intermediate nucleus of  the thalamus (Vim) and the zona incerta (ZI) have not yet been reported.Cases of  HT have been reported to respond to levodopa7 and to deep brain stimulation (DBS) of  several nuclei and structures, including the bilateral thalami,5 ventral Vim,8 subthalamic nucleus (STN), globus pal-lidus interna (GPi),2 and prelemniscal radiations (Raprl).9 The use of  the ZI target has been reported to be advantageous for treating more com-plex and proximal tremors,10 and has been previously reported as a tar-get to independently treat HT.11 The pathophysiology of  HT is complex, and it the combined dysfunction of  the pallidothalamic pathways that Columbia University LibrariesFreely available onlineTremor and Other Hyperkinetic Movementshttp://www.tremorjournal.orgAbstractBackground:  Holmes tremor (HT) arises from disruption of  the cerebellothalamocortical pathways. A lesion can interrupt the projection at any point, resulting in this tremor. We describe a case of  HT due to the rare artery of  Percheron infarct and its successful treatment using deep brain stimulation.Case report:  A 62-year-old woman with a right medial cerebral peduncle and bilateral thalamic stroke developed HT. Ventral intermediate nucleus (Vim) zona incerta (ZI) deep brain stimulation (DBS) surgery was performed, with improvement in her tremor.Discussion:  Our case supports the theory that the more caudal ZI target in combination with Vim is beneficial in treating poorly DBS-responsive tremors such as HT.Keywords: Deep brain stimulation, Holmes tremor, tremor, neurostimulationCitation: O’Shea SA, Elkind M, Pullman SL, Ford B. Holmes tremor due to artery of  percheron infarct: Clinical case and treatment using deep brain stimulation of  the Vim and ZI targets. Tremor Other Hyperkinet Mov. 2020; 10. doi: 10.7916/tohm.v0.732*To whom correspondence should be addressed. E-mail: soshea@bu.eduEditor: Elan D. Louis, Yale University, USAReceived: September 27, 2019; Accepted: December 05, 2019; Published: January 07, 2020Copyright: © 2020 O’Shea et al. This is an open-access article distributed under the terms of  the Creative Commons Attribution–Noncommercial–No Derivatives License, which per-mits the user to copy, distribute, and transmit the work provided that the original authors and source are credited; that no commercial use is made of  the work; and that the work is not altered or transformed.Funding: None.Financial Disclosures: None.Conflicts of Interest: The authors report no conflicts of  interest.Ethics Statement: This study was performed in accordance with the ethical standards detailed in the Declaration of  Helsinki. All patients that appear on video have provided written informed consent and authorization for videotaping and publication of  the videotape.O’Shea SA, Elkind M, Pullman SL, et al. Holmes Tremor and ViM/ZI DBSColumbia University LibrariesTremor and Other Hyperkinetic Movementshttp://www.tremorjournal.org 2necessitates implantation of  more than one target.11 Vim is known to be effective in treating distal limb tremors,2 and has been successfully used in treating HT in the setting of  TBI.2,3 ZI has been targeted in treatment of  more proximal tremors by overriding oscillations of  the interpositus nucleus (IO) and medial reticular formation (MRF). Given both the distal and proximal characteristics of  HT, combined Vim and ZI targets were pursued.10Case reportA 62-year-old right-handed woman presented to the Columbia University Movement Disorders Center for evaluation of  a rest tremor of  her left hand and leg that began 5 months after develop-ing a right medial cerebral peduncle and bilateral thalamic strokes. In addition to abnormal movements, her stroke symptoms included anterograde amnesia, fluctuating consciousness, somnolence, and vertical gaze palsy.Approximately 2.5 months after the onset of  tremor, a repeat MRI of  the brain was obtained, which revealed stable bilateral thalamic and right medial cerebral peduncle strokes (Figure 1). A DaT scan (I 123-FP CIT) was obtained, which revealed absent radiotracer activity in the right caudate and putamen, corresponding to the loca-tion of  her prior strokes. There was also reduced radiotracer uptake within the left putamen, with relatively preserved uptake in the left caudate (Figure 2), suggesting that in addition to the vascular insult A BFigure 1. Axial FLAIR MRI. Chronic infarcts of  the (A) right medial cerebellar peduncle and (B) bilateral thalami.Figure 2. DaT Scan (I 123-FP CIT). The Scan Demonstrates Absent Radiotracer Activity in the Right Caudate and Putamen and Reduced Radiotracer Uptake within the Left Putamen, with Relatively Preserved Uptake in the Left Caudate.O’Shea SA, Elkind M, Pullman SL, et al. Holmes Tremor and ViM/ZI DBSColumbia University LibrariesTremor and Other Hyperkinetic Movementshttp://www.tremorjournal.org 3contributing to her left-hand tremor, she may also have underlying presynaptic nigrostriatal dopaminergic dysfunction.Our examination, which was performed approximately 2 years after her ischemic stroke, revealed slightly reduced blink rate, mildly increased tone of  the left arm, and moderate rest tremor of  the left arm and leg. She had a mild kinetic tremor on the left, which inten-sified with posture, and was further exacerbated by movement. She also had a mild jaw tremor. Finger tapping, heel tapping, and rapid alternating movements were significant for slight decrementing of  amplitude on the left (total Unified Parkinson’s Disease Rating Scale, UPDRS, Part III score of  26).The patient was prescribed carbidopa-levodopa, with titration to a total of  1,500 mg/day. She reported significant improvement of  her tremor symptoms, notably in her follow-up examination during her clinical on-state. She had slight rest, postural, and kinetic tremor of  the left arm and no rest tremor of  the legs, and she was noted to have improved bradykinesia (total UPDRS Part III score of  11). The patient developed worsening somnolence while taking levodopa, however, and therefore underwent right Vim ZI DBS placement.Mapping and trajectory planning were performed with a volumet-ric CT scan preoperatively and fused to the MRI volumetric images using BrainLAB™ software. Permanent stimulating electrodes of  the Abbott St. Jude Medical Infinity™ DBS system were inserted with a guide sleeve through the Alpha Omega guidance system to just above the stereotactic target. The thalamic target was 11 mm lateral to the lateral wall of  the third ventricle and the ZI contact was below the anterior-to-posterior commissure plane.The patient did well postoperatively and was noted to have signifi-cant improvement of  her left arm tremors at rest, posture, and with movement, as well as subtle improvements in her bradykinesia on low output settings. She received symptomatic benefit after one program-ming session, which was approximately 2 weeks after her surgery, with optimal contacts at monopolar contact of  Case+ 2- (3.5 V; 140 Hz; 70 PW). Her UPDRS part III score postoperatively on these settings was 16 and 24 postoperatively when DBS was turned off  (see Video 1).Computerized spiral analysis was performed pre- and postopera-tively to quantify the effects of  DBS. This is a technique for measur-ing kinematic and other attributes of  spiral drawing12 that uses a digitizing tablet and computer and calculates a series of  mathemati-cal indices to assess upper limb motor function. Spiral analysis has been used to evaluate neurological disorders,13–17 to show motor learning in Essential Tremor (ET)18 and to help predict the responses to DBS in ET subjects.19 For this study, we used spiral analysis out-come measures with specific clinical relevance to tremor, parkinson-ism, and cerebellar dysfunction.Quantitative spiral analysis findings revealed overall improvement in measures of  upper limb motor execution post-DBS, though the left side still remained abnormal. There was clear improvement in tremors bilaterally, with lower tremor power, lower Degree of  Severity (DoS), improved secondary smoothness, and fewer tremor axes. Other measures remained the same or worsened slightly. Spiral loop width variability (SWVI), a measure of  ataxia, did not improve and remained high, indicative of  a cerebellar component to the tremors as well as associated with DBS resistance. It has also been suggested that tremors with high SWVI may not be optimally treated with Vim alone, and the addition of  ZI for such tremors should be considered.14,19–21 Tightness, a correlate of  micrographia, and draw-ing speed worsened slightly post-DBS, showing that some of  the par-kinsonian features of  this case were not affected (Figures 3 and 4; Table 1). Overall severity and number of  axes showed improvement, but tremor amplitude did not. This tremor profile is consistent with the previous finding that the DoS and tremor amplitude are separa-ble motor physiologic components in tremor that may be inde-pendently mediated.18The tremors in this subject were complex, with multiple axes, varying frequencies, drawing irregularity, and several other abnormal motor physiological features. Postoperatively in this subject, we found overall improvement in most, but not all, objective measures.Video 1.  The Patient is Evaluated Preoperatively without Levodopa in this Video. She is then evaluated postoperatively with the DBS turned on, then turned off. Note the improvement in the amplitude of  the tremor at rest, action, and posture when the DBS is turned on.BAFigure 3.  Axes Analysis: (A) Preoperatively  and (B) Postoperatively. Note the reduction in number and range of  tremor axes.O’Shea SA, Elkind M, Pullman SL, et al. Holmes Tremor and ViM/ZI DBSColumbia University LibrariesTremor and Other Hyperkinetic Movementshttp://www.tremorjournal.org 4DiscussionWe present a case of  a woman with onset of  levodopa-responsive HT secondary to a lesion of  the bilateral thalami and cerebral peduncle within the territory of  the AOP, who was successfully treated with Vim/ZI DBS. We believe this is also the first case report where quantitative spiral analysis was used to document objective details of  the motoric changes, revealing improvement in several kinematic features of  spiral drawing, as well as lack of  improvement in other features. There were asymmetric DaT scan findings, which suggest possible underlying presynaptic nigrostriatal dopaminergic dysfunction in addition to the vascular lesion of  the thalamus.Prior reports of  HT with underlying parkinsonism have been reported9; however, the treatment of  HT that is associated with vascular injury in the distribution of  the AOP with Vim and ZI DBS targets has not yet been reported. Although prior reports have suggested treatment of  HT with Vim and ZI targets independently, the addition of  ZI to treat this particularly treatment-resistant tremor has not yet been used and should be considered in patients with complex and difficult-to-treat tremors such as HT.BAFigure 4. Tremor Analysis Spirals of  the Left, Nondominant Hand. (A) Preoperative and (B) Postoperative Spirals.O’Shea SA, Elkind M, Pullman SL, et al. Holmes Tremor and ViM/ZI DBSColumbia University LibrariesTremor and Other Hyperkinetic Movementshttp://www.tremorjournal.org 5References1. Deuschl, G, Bain, P, Brin, M, an Ad Hoc Scientific Committee of  the Movement Disorders Society. Consensus statement of  the Movements Disorders Society on Tremor. Mov Disord 1998;13(Suppl 3):2–23. doi: 10.1002/mds.8701313032. Foote KD, Okun MS. Ventralis intermedius plus ventralis oralis anterior and posterior deep brain stimulation for posttraumatic Holmes tremor: two leads may be better than one: technical note. Neurosurgery 2005;56(2 Suppl):E445. doi: 10.1227/01.neu.0000157104.87448.783. Follett MA, Torres-Russotto D, Follett KA. Bilateral deep brain stimulation of  the ventral intermediate nucleus of  the thalamus for posttraumatic midbrain tremor. Neuromodulation 2014;17(3):289–291. doi: 10.1111/ner.120964. Alqwaifly M. Treatment responsive Holmes tremor: case report and litera-ture review. Int J Health Sci 2016;10(4):558–562. PMCID: PMC5085351.5. Kudo M, Goto S, Nishikawa S, Hamasaki T, Soyama N, Ushio Y, et al. Bilateral thalamic stimulation for Holmes’ tremor caused by unilateral brainstem lesion. Mov Disord 2001;16(1):170–174. PMID: 29904635.6. Bejr-Kasem Marco H, Lorenzo-Bosquet C, Alvarez-Sabín J, Hernández-Vara J. Parkinsonism related to Percheron artery infarct. J Neurol Sci 2017;373:21–22. doi: 10.1016/j.jns.2016.12.0117. Raina GB, Cersosimo MG, Folgar SS, Giugni JC, Calandra C, Paviolo JP. Holmes tremor. Clinical description, lesion localization, and treatment in a series of  29 cases. Neurology 2016;86(10):931–938. doi: 10.1212/WNL.000000000 00024408. Romanelli P, Brontë-Stewart H, Courtney T, Heit G. Possible necessity for deep brain stimulation of  both the ventralis intermedius and subthalamic nuclei to resolve Holmes tremor. Case report. J Neurosurg 2003;99(3):566–571. doi: 10.3171/jns.2003.99.3.0566.9. Martinez V, Hu S-C, Foutz TJ, Ko A. Successful treatment of  Holmes tremor with deep brain stimulation of  the prelemniscal radiations. Front Surg 2018;5:21. doi: 10.3389/fsurg.2018.00021.10. Avila A, Caballol N, Marti, M. Simultaneous classical and Holmes’ tremor in Parkinson’s disease: involvement of  the cerebellum. Can J Neurol Sci 2017;44:436–440. doi: 10.1017/cjn.2016.45111. Plaha P, Khan S, Javed S, Gill S. Caudal zona incerta as an alternative target for the treatment of  tremor with deep brain stimulation. Eur Neurol Rev 2009;4(1):91–96. doi: 10.17925/ENR.2009.04.01.9112. Pullman SL. Spiral analysis: a new technique for measuring tremor with a digitizing tablet. Mov Disord 1998;13(Suppl 3):85–89. doi: 10.1002/mds. 87013131513. Haubenberger D, Kalowitz D, Nahab FB, Toro C, Ippolito D, Luckenbaugh DA, et al. Validation of  digital spiral analysis as outcome parameter for clinical trials in essential tremor. Mov Disord 2011;26(11): 2073–2080. doi: 10.1002/mds.2380814. Louis ED, Gillman A, Boschung S, Hess CW, Yu Q, Pullman SL. High width variability during spiral drawing: further evidence of  cerebellar  dysfunction in essential tremor. Cerebellum 2012;11(4):872–879. doi: 10.1007/s12311-011-0352-415. San Luciano M, Wang C, Ortega RA, Yu Q, Boschung S, Soto-Valencia J, et al. Digitized spiral drawing: a possible biomarker for early Parkinson’s dis-ease. PLoS One 2016;11(10):e0162799. doi: 10.1371/journal.pone.016279916. Hsu AW, Piboolnurak PA, Floyd AG, Yu QP, Wraith JE, Patterson MC, et al. Spiral analysis in Niemann-Pick disease type C. Mov Disord 2009; 24(13):1984–1990. doi: 10.1002/mds.2274417. Ratliff  J, Ortega RA, Ooi HY, Mirallave A, Glickman A, Yu Q, et al. Digitized spiral analysis may be a potential biomarker for brachial dystonia. Parkinsonism Relat Disord 2018 ;57:16–21. doi: 10.1016/j.parkreldis.2018.07.004Table 1.  Key Tremor Axes Analysis (Top) and Spiral Analysis (Bottom) Findings of  the Left, Nondominant Hand, Pre- and PostoperativelyPre-DBS Post-DBSAxes Frequency range (in Hz) 3.74–7.17 3.27–3.77 Primary axes range (in degrees) 40–115 50–90Tremor Degree of  Severity 2.872 ± 0.288 2.678 ± 0.327 Tremor frequency 5.090 ± 0.152 3.506 ± 0.074 Max power 4.830 ± 1.862 3.909 ± 0.055 Amplitude (cm) 3.065 ± 0.861 4.370 ± 1.367 Tightness 0.979 ± 0.057 1.295 ± 0.109 Width variation 0.493 ± 0.104 0.497 ± 0.073 Second-order smoothness 1.873 ± 1.206 −0.133 ± 1.631Abbreviation: DBS, Deep Brain Stimulation.Note the reduction in frequency range in the axes analysis. Also note the reduction in tremor power and Degree of  Severity (DoS) postoperatively, as well as the improvement in second-order smoothness (negative values indicate improved execution of  spiral drawing, with the normal value being −4.19). Spiral loop width variability is indicated by “width variation” is indicative of  cerebellar dysfunction and did not significantly change postoperatively.O’Shea SA, Elkind M, Pullman SL, et al. Holmes Tremor and ViM/ZI DBSColumbia University LibrariesTremor and Other Hyperkinetic Movementshttp://www.tremorjournal.org 618. Kim CY, Luo L, Yu Q, Mirallave A, Saunders-Pullman R, Lipton RB, et al. Repeated spiral drawings in essential tremor: a possible limb-based measure of  motor learning. Cerebullum 2019;18(2):178–187. doi: 10.1007/s12311-018-0974-x19. Merchant SH, Kuo SH, Qiping Y, Winfield L, McKhann G, Sheth S, et al. Objective predictors of  “early tolerance” to ventral intermediate nucleus of  thal-amus deep brain stimulation in essential tremor patients Clin Neurophysiol 2018;129(8):1628–1633. doi: 10.1016/j.clinph.2018.05.01220. Blomstedt P, Sandvik U, Linder J, Fredricks A, Forsgren L, Hariz MI. Deep brain stimulation of  the subthalamic nucleus versus the zona incerta in the treat-ment of  essential tremor. Acta Neurochir (Wien) 2011;153(12): 2329–2335. doi: 10.1007/s00701-011-1157-421. Hess CW, Pullman SL. Tremor: clinical phenomenology and assessment techniques. Tremor Other Hyperkinet Mov (N Y) 2012;2:tre-02-65-365-1. doi: 10.7916/D8WM1C41

Holmes Tremor due to Artery of Percheron Infarct: Clinical Case and Treatment Using Deep Brain Stimulation of the Vim and ZI Targets

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Holmes Tremor due to Artery of Percheron Infarct: Clinical Case and Treatment Using Deep Brain Stimulation of the Vim and ZI Targets

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