Indications and approaches for functional neurosurgery in multiple sclerosis, including the role for lesional surgery and deep brain stimulation

Main Article Content

Holly Roy Tipu Aziz

Abstract

Multiple sclerosis is a chronic and disabling condition of the central nervous system, associated with variable and wide-ranging symptoms. In some patients, functional neurosurgery may be considered for the relief of symptoms including tremor and pain. This could include lesional surgery or deep brain stimulation. In this review we evaluate the evidence for lesional neurosurgery and deep brain stimulation in multiple sclerosis, comparing these approaches and associated outcomes, and identifying the key symptoms which are thought to be amenable to intervention.


 

Article Details

How to Cite
ROY, Holly; AZIZ, Tipu. Indications and approaches for functional neurosurgery in multiple sclerosis, including the role for lesional surgery and deep brain stimulation. Medical Research Archives, [S.l.], v. 8, n. 6, june 2020. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/2147>. Date accessed: 21 nov. 2024. doi: https://doi.org/10.18103/mra.v8i6.2147.
Section
Research Articles

References

1 Noseworthy, J. H., Lucchinetti, C., Rodriguez, M. & Weinshenker, B. G. Multiple sclerosis. The New England journal of medicine 2000; 343, 938-952
2 Lindsat, K., Bone, I. & Fuller, G. Neurology and Neurosurgery Illustrated. 5th edn, (Elsevier, 2010).
3 Bain, P., Aziz, T., Liu, X. & Nandi, D. Deep Brain Stimulation. (Oxford University Press, 2009).
4 Boonstra, F. M., Noffs G., Perera T. et al. Functional neuroplasticity in response to cerebello-thalamic injury underpins the clinical presentation of tremor in multiple sclerosis. Mult Scler 2019; 1352458519837706, doi:10.1177/1352458519837706
5 Pittock, S. J., McClelland, R. L., Mayr, W. T., Rodriguez, M. & Matsumoto, J. Y. Prevalence of tremor in multiple sclerosis and associated disability in the Olmsted County population. Movement disorders : official journal of the Movement Disorder Society 2004; 19, 1482-1485, doi:10.1002/mds.20227
6 Herzog, J. Hamel, W., Wenzelburger R., et al. Kinematic analysis of thalamic versus subthalamic neurostimulation in postural and intention tremor. Brain : a journal of neurology 2007; 130, 1608-1625, doi:10.1093/brain/awm077
7 Kocabicak, E., Terzi, M., Alptekin, O. & Temel, Y. Targeting thalamic tremor cells in deep brain stimulation for multiple sclerosis-induced complex tremor. Surgical neurology international 2013; 4, 31, doi:10.4103/2152-7806.109464
8 Van Der Walt, A., Sung, S., Spelman, T., et al. A double-blind, randomized, controlled study of botulinum toxin type A in MS-related tremor. Neurology 2012; 79, 92-99, doi:10.1212/WNL.0b013e31825dcdd9
9 Bozek, C. B., Kastrukoff, L. F., Wright, J. M., Perry, T. L. & Larsen, T. A. A controlled trial of isoniazid therapy for action tremor in multiple sclerosis. Journal of neurology 1987; 234, 36-39
10 Hallett, M., Lindsey, J. W., Adelstein, B. D. & Riley, P. O. Controlled trial of isoniazid therapy for severe postural cerebellar tremor in multiple sclerosis. Neurology 1985; 35, 1374-1377
11 Cooper, I. S. Relief of intention tremor of multiple sclerosis by thalamic surgery. Jama 1967; 199, 689-694
12 Feys, P., Maes, F., Nuttin, B et al. Relationship between multiple sclerosis intention tremor severity and lesion load in the brainstem. Neuroreport 2005; 16, 1379-1382, doi:10.1097/01.wnr.0000176521.26971.58
13 Cooper, I. S. Neurosurgical alleviation of intention tremor of multiple sclerosis and cerebellar disease. The New England journal of medicine 1960; 263, 441-444, doi:10.1056/NEJM196009012630905
14 Alusi, S. H., Worthington, J., Glickman, S. & Bain, P. G. A study of tremor in multiple sclerosis. Brain : a journal of neurology 2001; 124, 720-730, doi:10.1093/brain/124.4.720
15 Speelman, J. D. & Van Manen, J. Stereotactic thalamotomy for the relief of intention tremor of multiple sclerosis. Journal of neurology, neurosurgery, and psychiatry 1984; 47, 596-599, doi:10.1136/jnnp.47.6.596
16 Critchley, G. R. & Richardson, P. L. Vim thalamotomy for the relief of the intention tremor of multiple sclerosis. British journal of neurosurgery 1998; 12, 559-562, doi:10.1080/02688699844439
17 Alusi, S. H. et al. Stereotactic lesional surgery for the treatment of tremor in multiple sclerosis: a prospective case-controlled study. Brain : a journal of neurology 2001; 124, 1576-1589, doi:10.1093/brain/124.8.1576
18 Whittle, I. R. & Haddow, L. J. CT guided thalamotomy for movement disorders in multiple sclerosis: problems and paradoxes. Acta neurochirurgica. Supplement 1995; 64, 13-16, doi:10.1007/978-3-7091-9419-5_4
19 Broager, B. & Fog, T. Thalamotomy for the relief of intention tremor in multiple sclerosis. Acta neurologica Scandinavica. Supplementum 1962; 38, 153-156, doi:10.1111/j.1600-0404.1962.tb01135.x
20 Bittar, R. G. et al. Thalamotomy versus thalamic stimulation for multiple sclerosis tremor. Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia 2005; 12, 638-642, doi:10.1016/j.jocn.2004.09.008
21 Krayenbuehl, H. & Yasargil, M. G. Relief of intention tremor due to multiple sclerosis by stereotaxic thalamotomy. Confinia neurologica 1962; 22, 368-374, doi:10.1159/000104388
22 Mathieu, D., Kondziolka, D., Niranjan, A., Flickinger, J. & Lunsford, L. D. Gamma knife thalamotomy for multiple sclerosis tremor. Surgical neurology 2007; 68, 394-399, doi:10.1016/j.surneu.2006.11.049
23 Elias, W. J. Lipsman, N., Ondo, W. G., et al. A Randomized Trial of Focused Ultrasound Thalamotomy for Essential Tremor. The New England journal of medicine 2016; 375, 730-739, doi:10.1056/NEJMoa1600159
24 Lipsman, N. Schwartz M.L. Huang, Y., et al. MR-guided focused ultrasound thalamotomy for essential tremor: a proof-of-concept study. The Lancet. Neurology 2013; 12, 462-468, doi:10.1016/S1474-4422(13)70048-6
25 Manez-Miro, J. U. Martinez-Fernandez. R., del Alamo. M., et al. Focused ultrasound thalamotomy for multiple sclerosis-associated tremor. Mult Scler 2019; doi:10.1177/1352458519861597
26 Brice, J. & McLellan, L. Suppression of intention tremor by contingent deep-brain stimulation. Lancet 1980; 315, 1221-1222
27 Koch, M., Mostert, J., Heersema, D. & De Keyser, J. Tremor in multiple sclerosis. Journal of neurology 2007; 254, 133-145, doi:10.1007/s00415-006-0296-7
28 Brandmeir, N. J., Murray, A., Cheyuo, C., Ferari, C. & Rezai, A. R. Deep Brain Stimulation for Multiple Sclerosis Tremor: A Meta-Analysis. Neuromodulation : journal of the International Neuromodulation Society. 2019; doi:10.1111/ner.13063
29 Nandi, D. & Aziz, T. Z. Deep brain stimulation in the management of neuropathic pain and multiple sclerosis tremor. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society 2004; 21, 31-39, doi:10.1097/00004691-200401000-00005
30 Berk, C., Carr, J., Sinden, M., Martzke, J. & Honey, C. R. Thalamic deep brain stimulation for the treatment of tremor due to multiple sclerosis: a prospective study of tremor and quality of life. Journal of neurosurgery 2002; 97, 815-820, doi:10.3171/jns.2002.97.4.0815
31 Zakaria, R., Vajramani G., Westmoreland, L. et al. Tremor reduction and quality of life after deep brain stimulation for multiple sclerosis-associated tremor. Acta neurochirurgica 2013; 155, 2359-2364; discussion 2364, doi:10.1007/s00701-013-1848-0
32 Geny, C., Nguyen J-P., Pollin. B., et al. Improvement of severe postural cerebellar tremor in multiple sclerosis by chronic thalamic stimulation. Movement disorders : official journal of the Movement Disorder Society. 1996; 11, 489-494, doi:10.1002/mds.870110503
33 Thevathasan, W., Schweder, P., Joint, C., et al. Permanent tremor reduction during thalamic stimulation in multiple sclerosis. Journal of neurology, neurosurgery, and psychiatry 2011; 82, 419-422, doi:10.1136/jnnp.2010.213900
34 Hyam, J. A., Aziz, T. Z. & Bain, P. G. Post-deep brain stimulation--gradual non-stimulation dependent decrease in strength with attenuation of multiple sclerosis tremor. Journal of neurology 2007; 254, 854-860, doi:10.1007/s00415-006-0433-3
35 Benabid, A. L., Pollak, P., Gao, D., et al. Chronic electrical stimulation of the ventralis intermedius nucleus of the thalamus as a treatment of movement disorders. Journal of neurosurgery 1996; 84, 203-214, doi:10.3171/jns.1996.84.2.0203.
36 Schuurman, P. R. Bosch, D. A., Merkus, M. P., et al. A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. The New England journal of medicine 2000; 342, 461-468, doi:10.1056/NEJM200002173420703
37 Plaha, P., Khan, S. & Gill, S. S. Bilateral stimulation of the caudal zona incerta nucleus for tremor control. Journal of neurology, neurosurgery, and psychiatry 2008; 79, 504-513, doi:10.1136/jnnp.2006.112334
38 Oliveria, S. F., Rodriguez, R.L., Bowers, D., et al. Safety and efficacy of dual-lead thalamic deep brain stimulation for patients with treatment-refractory multiple sclerosis tremor: a single-centre, randomised, single-blind, pilot trial. The Lancet. Neurology 2017; 16, 691-700, doi:10.1016/S1474-4422(17)30166-7
39 Altinel, Y., Alkhalfan, F., Qiao, N. & Velimirovic, M. Outcomes in Lesion Surgery versus Deep Brain Stimulation in Patients with Tremor: A Systematic Review and Meta-Analysis. World neurosurgery 2019; 123, 443-452 e448, doi:10.1016/j.wneu.2018.11.175
40 Schuurman, P. R., Bosch, D. A., Merkus, M. P. & Speelman, J. D. Long-term follow-up of thalamic stimulation versus thalamotomy for tremor suppression. Movement disorders : official journal of the Movement Disorder Society 2008; 23, 1146-1153, doi:10.1002/mds.22059
41 Akram, H. Dayal, V., Mahlknecht, P. et al. Connectivity derived thalamic segmentation in deep brain stimulation for tremor. NeuroImage. Clinical 2008; 18, 130-142, doi:10.1016/j.nicl.2018.01.008
42 Su, J. H., Thomas, F. T., Kasoff, W. F., et al. Thalamus Optimized Multi Atlas Segmentation (THOMAS): fast, fully automated segmentation of thalamic nuclei from structural MRI. NeuroImage 2019; 194, 272-282, doi:10.1016/j.neuroimage.2019.03.021
43 Igarashi, A., Tanaka, M., Abe, K. et al. Cost-minimisation model of magnetic resonance-guided focussed ultrasound therapy compared to unilateral deep brain stimulation for essential tremor treatment in Japan. PloS one 2019; 14, e0219929, doi:10.1371/journal.pone.0219929
44 Yap, L., Kouyialis, A. & Varma, T. R. Stereotactic neurosurgery for disabling tremor in multiple sclerosis: thalamotomy or deep brain stimulation? British journal of neurosurgery 2007; 21, 349-354, doi:10.1080/02688690701544002
45 Kalia, L. V. & O'Connor, P. W. Severity of chronic pain and its relationship to quality of life in multiple sclerosis. Mult Scler 2005; 11, 322-327
46 Heitmann, H., Haller, B., Tiemann, L., et al. Longitudinal prevalence and determinants of pain in multiple sclerosis: results from the German National Multiple Sclerosis Cohort study. Pain 2020; 161, 787-796, doi:10.1097/j.pain.0000000000001767
47 Poncet-Megemont, L., Dallel, R., Chassain, C. et al. Whole-body reversible neuropathic pain associated with right parieto-temporal operculum single inflammatory lesion in a patient with multiple sclerosis: A case report. Eur J Pain 2019; 23, 1763-1766, doi:10.1002/ejp.1464
48 Nomura, S., Shimakawa S., Kashiwagi, M. et al. Acute abdominal pain as the only symptom of a thoracic demyelinating lesion in multiple sclerosis. Brain & development 2015; 37, 983-987, doi:10.1016/j.braindev.2015.03.006
49 Hosobuchi, Y., Adams, J. E. & Rutkin, B. Chronic thalamic stimulation for the control of facial anesthesia dolorosa. Archives of neurology 1973; 29, 158-161
50 Hosobuchi, Y., Adams, J. E. & Linchitz, R. Pain relief by electrical stimulation of the central gray matter in humans and its reversal by naloxone. Science 1977; 197, 183-186
51 Richardson, D. E. & Akil, H. Long term results of periventricular gray self-stimulation. Neurosurgery 1977; 1, 199-202
52 Green, A. L., Nandi, D., Armstrong, G., Carter, H. & Aziz, T. Post-herpetic trigeminal neuralgia treated with deep brain stimulation. Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia 2003; 10, 512-514
53 Boccard, S. G., Pereira, E. A., Moir, L., Aziz, T. Z. & Green, A. L. Long-term outcomes of deep brain stimulation for neuropathic pain. Neurosurgery. 2013; 72, 221-230; discussion 231, doi:10.1227/NEU.0b013e31827b97d6
54 Cordella, R., Franzini, A., La Mantia, L. et al. Hypothalamic stimulation for trigeminal neuralgia in multiple sclerosis patients: efficacy on the paroxysmal ophthalmic pain. Mult Scler 2009; 15, 1322-1328, doi:10.1177/1352458509107018
55 Pereira, E. A., Vaz R., Rebelo, V., et al. Thalamic deep brain stimulation for neuropathic pain after amputation or brachial plexus avulsion. Neurosurgical focus 2013; 35, E7, doi:10.3171/2013.7.FOCUS1346
56 Love, S. & Coakham, H. B. Trigeminal neuralgia: pathology and pathogenesis. Brain : a journal of neurology. 2001; 124, 2347-2360
57 Laakso, S. M. et al. Trigeminal neuralgia in multiple sclerosis: Prevalence and association with demyelination. Acta neurologica Scandinavica 2020; doi:10.1111/ane.13243
58 Fowler, C. J., Panicker, J. N., Drake, M., et al. A UK consensus on the management of the bladder in multiple sclerosis. Journal of neurology, neurosurgery, and psychiatry 2009; 80, 470-477, doi:10.1136/jnnp.2008.159178
59 De Ridder, D., Van Der Aa, F., Debruyne J., et al. Consensus guidelines on the neurologist's role in the management of neurogenic lower urinary tract dysfunction in multiple sclerosis. Clinical neurology and neurosurgery 2013; doi:10.1016/j.clineuro.2013.06.018
60 Green, A. L., Stone E., Sitsapsan, H., et al. Switching off micturition using deep brain stimulation at midbrain sites. Annals of neurology 2012; 72, 144-147, doi:10.1002/ana.23571
61 Finazzi-Agro, E., Peppe, A., D'Amico A. et al. Effects of subthalamic nucleus stimulation on urodynamic findings in patients with Parkinson's disease. The Journal of urology 2003; 169, 1388-1391, doi:10.1097/01.ju.0000055520.88377.dc
62 Mordasini, L., Kessler, T. M., Kiss, B. et al. Bladder function in patients with dystonia undergoing deep brain stimulation. Parkinsonism & related disorders 2014; 20, 1015-1017, doi:10.1016/j.parkreldis.2014.05.016
63 Porter, R. W. A pallidal response to detrusor contraction. Brain research 4, 381-383, doi:10.1016/0006-8993(67)90169-2 (1967).
64 Roy, H. A., Aziz, T. Z., Fitzgerald, J. J. & Green, A. L. Beta oscillations and urinary voiding in Parkinson disease. Neurology 2018; 90, e1530-e1534, doi:10.1212/WNL.0000000000005355
65 Montgomery, E. B., Jr., Baker, K. B., Kinkel, R. P. & Barnett, G. Chronic thalamic stimulation for the tremor of multiple sclerosis. Neurology 1999; 53, 625-628, doi:10.1212/wnl.53.3.625
66 Moore, G. R., Vitali, A. M., Leung, E., et al. Thalamic stimulation in multiple sclerosis: evidence for a 'demyelinative thalamotomy'. Mult Scler 2009; 15, 1311-1321, doi:10.1177/1352458509345914
67 Ortiz, F. C., Habermacher, C., Graciarena, M., et al. Neuronal activity in vivo enhances functional myelin repair. JCI insight 2019; 5, doi:10.1172/jci.insight.123434
68 McLean, N. A., Popescu, B. F., Gordon, T., Zochodne, D. W. & Verge, V. M. Delayed nerve stimulation promotes axon-protective neurofilament phosphorylation, accelerates immune cell clearance and enhances remyelination in vivo in focally demyelinated nerves. PloS one 9, e110174, doi:10.1371/journal.pone.0110174 (2014).