Rates and Predictors of Pain Reduction With Intracranial Stimulation for Intractable Pain Disorders.
Journal
Neurosurgery
ISSN: 1524-4040
Titre abrégé: Neurosurgery
Pays: United States
ID NLM: 7802914
Informations de publication
Date de publication:
05 Jun 2024
05 Jun 2024
Historique:
received:
29
12
2023
accepted:
01
04
2024
medline:
5
6
2024
pubmed:
5
6
2024
entrez:
5
6
2024
Statut:
aheadofprint
Résumé
Intracranial modulation paradigms, namely deep brain stimulation (DBS) and motor cortex stimulation (MCS), have been used to treat intractable pain disorders. However, treatment efficacy remains heterogeneous, and factors associated with pain reduction are not completely understood. We performed an individual patient review of pain outcomes (visual analog scale, quality-of-life measures, complications, pulse generator implant rate, cessation of stimulation) after implantation of DBS or MCS devices. We evaluated 663 patients from 36 study groups and stratified outcomes by pain etiology and implantation targets. Included studies comprised primarily retrospective cohort studies. MCS patients had a similar externalized trial success rate compared with DBS patients (86% vs 81%; P = .16), whereas patients with peripheral pain had a higher trial success rate compared with patients with central pain (88% vs 79%; P = .004). Complication rates were similar for MCS and DBS patients (12% vs 15%; P = .79). Patients with peripheral pain had lower likelihood of device cessation compared with those with central pain (5.7% vs 10%; P = .03). Of all implanted patients, mean pain reduction at last follow-up was 45.8% (95% CI: 40.3-51.2) with a 31.2% (95% CI: 12.4-50.1) improvement in quality of life. No difference was seen between MCS patients (43.8%; 95% CI: 36.7-58.2) and DBS patients (48.6%; 95% CI: 39.2-58) or central (41.5%; 95% CI: 34.8-48.2) and peripheral (46.7%; 95% CI: 38.9-54.5) etiologies. Multivariate analysis identified the anterior cingulate cortex target to be associated with worse pain reduction, while postherpetic neuralgia was a positive prognostic factor. Both DBS and MCS have similar efficacy and complication rates in the treatment of intractable pain. Patients with central pain disorders tended to have lower trial success and higher rates of device cessation. Additional prognostic factors include anterior cingulate cortex targeting and postherpetic neuralgia diagnosis. These findings underscore intracranial neurostimulation as an important modality for treatment of intractable pain disorders.
Sections du résumé
BACKGROUND AND OBJECTIVES
OBJECTIVE
Intracranial modulation paradigms, namely deep brain stimulation (DBS) and motor cortex stimulation (MCS), have been used to treat intractable pain disorders. However, treatment efficacy remains heterogeneous, and factors associated with pain reduction are not completely understood.
METHODS
METHODS
We performed an individual patient review of pain outcomes (visual analog scale, quality-of-life measures, complications, pulse generator implant rate, cessation of stimulation) after implantation of DBS or MCS devices. We evaluated 663 patients from 36 study groups and stratified outcomes by pain etiology and implantation targets.
RESULTS
RESULTS
Included studies comprised primarily retrospective cohort studies. MCS patients had a similar externalized trial success rate compared with DBS patients (86% vs 81%; P = .16), whereas patients with peripheral pain had a higher trial success rate compared with patients with central pain (88% vs 79%; P = .004). Complication rates were similar for MCS and DBS patients (12% vs 15%; P = .79). Patients with peripheral pain had lower likelihood of device cessation compared with those with central pain (5.7% vs 10%; P = .03). Of all implanted patients, mean pain reduction at last follow-up was 45.8% (95% CI: 40.3-51.2) with a 31.2% (95% CI: 12.4-50.1) improvement in quality of life. No difference was seen between MCS patients (43.8%; 95% CI: 36.7-58.2) and DBS patients (48.6%; 95% CI: 39.2-58) or central (41.5%; 95% CI: 34.8-48.2) and peripheral (46.7%; 95% CI: 38.9-54.5) etiologies. Multivariate analysis identified the anterior cingulate cortex target to be associated with worse pain reduction, while postherpetic neuralgia was a positive prognostic factor.
CONCLUSION
CONCLUSIONS
Both DBS and MCS have similar efficacy and complication rates in the treatment of intractable pain. Patients with central pain disorders tended to have lower trial success and higher rates of device cessation. Additional prognostic factors include anterior cingulate cortex targeting and postherpetic neuralgia diagnosis. These findings underscore intracranial neurostimulation as an important modality for treatment of intractable pain disorders.
Identifiants
pubmed: 38836613
doi: 10.1227/neu.0000000000003006
pii: 00006123-990000000-01186
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © Congress of Neurological Surgeons 2024. All rights reserved.
Références
Szymoniuk M, Chin JH, Domagalski Ł, Biszewski M, Jóźwik K, Kamieniak P. Brain stimulation for chronic pain management: a narrative review of analgesic mechanisms and clinical evidence. Neurosurg Rev. 2023;46(1):127.
Frizon LA, Yamamoto EA, Nagel SJ, Simonson MT, Hogue O, Machado AG. Deep brain stimulation for pain in the modern era: a systematic review. Neurosurgery. 2020;86(2):191-202.
Coffey RJ. Deep brain stimulation for chronic pain: results of two multicenter trials and a structured review. Pain Med. 2001;2(3):183-192.
Levy RM, Lamb S, Adams JE. Treatment of chronic pain by deep brain stimulation: long term follow-up and review of the literature. Neurosurgery. 1987;21(6):885-893.
Pycroft L, Stein J, Aziz T. Deep brain stimulation: an overview of history, methods, and future developments. Brain Neurosci Adv. 2018;2:2398212818816017.
Abdallat M, Saryyeva A, Blahak C, et al. Centromedian-parafascicular and somatosensory thalamic deep brain stimulation for treatment of chronic neuropathic pain: a contemporary series of 40 patients. Biomedicines. 2021;9(7):731.
Nowacki A, Zhang D, Barlatey S, et al. Deep brain stimulation of the central lateral and ventral posterior thalamus for central poststroke pain syndrome: preliminary experience. Neuromodulation. 2023;26(8):1747-1756.
Boccard SGJ, Fernandes HM, Jbabdi S, et al. Tractography study of deep brain stimulation of the anterior cingulate cortex in chronic pain: key to improve the targeting. World Neurosurg. 2016;86:361.e1-3-370.e1-3.
Hunsche S, Sauner D, Runge MJR, et al. Tractography-guided stimulation of somatosensory fibers for thalamic pain relief. Stereotact Funct Neurosurg. 2013;91(5):328-334.
Tsubokawa T, Katayama Y, Yamamoto T, Hirayama T, Koyama S. Chronic motor cortex stimulation for the treatment of central pain. Acta Neurochir Suppl. 1991;52:137-139.
Ramos-Fresnedo A, Perez-Vega C, Domingo RA, Cheshire WP, Middlebrooks EH, Grewal SS. Motor cortex stimulation for pain: a narrative review of indications, techniques, and outcomes. Neuromodulation. 2022;25(2):211-221.
Wang D, Lu Y, Han Y, et al. The influence of etiology and stimulation target on the outcome of deep brain stimulation for chronic neuropathic pain: a systematic review and meta-analysis. Neuromodulation. 2024;27(1):83-94.
Levy R, Deer TR, Henderson J. Intracranial neurostimulation for pain control: a review. Pain Physician. 2010;13(2):157-165.
Guo S, Zhang X, Tao W, Zhu H, Hu Y. Long-term follow-up of motor cortex stimulation on central poststroke pain in thalamic and extrathalamic stroke. Pain Pract. 2022;22(7):610-620.
Zhang X, Zhu H, Tao W, Li Y, Hu Y. Motor cortex stimulation therapy for relief of central post-stroke pain: a retrospective study with neuropathic pain symptom inventory. Stereotact Funct Neurosurg. 2018;96(4):239-243.
Zhang X, Hu Y, Tao W, Zhu H, Xiao D, Li Y. The effect of motor cortex stimulation on central poststroke pain in a series of 16 patients with a mean follow-up of 28 months. Neuromodulation. 2017;20(5):492-496.
Pommier B, Quesada C, Fauchon C, Nuti C, Vassal F, Peyron R. Added value of multiple versus single sessions of repetitive transcranial magnetic stimulation in predicting motor cortex stimulation efficacy for refractory neuropathic pain. J Neurosurg. 2018;130(5):1750-1761.
Pommier B, Quesada C, Nuti C, Peyron R, Vassal F. Is the analgesic effect of motor cortex stimulation somatotopically driven or not? Neurophysiol Clin. 2020;50(3):195-203.
Ben-Haim S, Mirzadeh Z, Rosenberg WS. Deep brain stimulation for intractable neuropathic facial pain. Neurosurg Focus. 2018;45(2):e15.
Brown JA, Pilitsis JG. Motor cortex stimulation for central and neuropathic facial pain: a prospective study of 10 patients and observations of enhanced sensory and motor function during stimulation. Neurosurgery. 2005;56(2):290-297; discussion 290-297.
Hamani C, Schwalb JM, Rezai AR, Dostrovsky JO, Davis KD, Lozano AM. Deep brain stimulation for chronic neuropathic pain: long-term outcome and the incidence of insertional effect. Pain. 2006;125(1-2):188-196.
Pirotte B, Voordecker P, Neugroschl C, et al. Combination of functional magnetic resonance imaging-guided neuronavigation and intraoperative cortical brain mapping improves targeting of motor cortex stimulation in neuropathic pain. Neurosurgery. 2008;62(6 Suppl 3):941-956.
Velasco F, Carrillo-Ruiz JD, Castro G, et al. Motor cortex electrical stimulation applied to patients with complex regional pain syndrome. Pain. 2009;147(1-3):91-98.
Velasco F, Argüelles C, Carrillo-Ruiz JD, et al. Efficacy of motor cortex stimulation in the treatment of neuropathic pain: a randomized double-blind trial. J Neurosurg. 2008;108(4):698-706.
Lefaucheur JP, Keravel Y, Nguyen JP. Treatment of poststroke pain by epidural motor cortex stimulation with a new octopolar lead. Neurosurgery. 2011;68(1 Suppl Operative):180-187; discussion 187.
Lefaucheur JP, Drouot X, Cunin P, et al. Motor cortex stimulation for the treatment of refractory peripheral neuropathic pain. Brain. 2009;132(Pt 6):1463-1471.
Nguyen JP, Velasco F, Brugières P, et al. Treatment of chronic neuropathic pain by motor cortex stimulation: results of a bicentric controlled crossover trial. Brain Stimul. 2008;1(2):89-96.
Holsheimer J, Lefaucheur JP, Buitenweg JR, Goujon C, Nineb A, Nguyen JP. The role of intra-operative motor evoked potentials in the optimization of chronic cortical stimulation for the treatment of neuropathic pain. Clin Neurophysiol. 2007;118(10):2287-2296.
Rasche D, Tronnier VM. Clinical significance of invasive motor cortex stimulation for trigeminal facial neuropathic pain syndromes. Neurosurgery. 2016;79(5):655-666.
Rasche D, Rinaldi PC, Young RF, Tronnier VM. Deep brain stimulation for the treatment of various chronic pain syndromes. Neurosurg Focus. 2006;21(6):e8.
Rasche D, Ruppolt M, Stippich C, Unterberg A, Tronnier VM. Motor cortex stimulation for long-term relief of chronic neuropathic pain: a 10 year experience. Pain. 2006;121(1-2):43-52.
Elias GJB, De Vloo P, Germann J, et al. Mapping the network underpinnings of central poststroke pain and analgesic neuromodulation. Pain. 2020;161(12):2805-2819.
Lavrov I, Latypov T, Mukhametova E, et al. Pre-motor versus motor cerebral cortex neuromodulation for chronic neuropathic pain. Sci Rep. 2021;11(1):12688.
Hollingworth M, Sims-Williams HP, Pickering AE, Barua N, Patel NK. Single electrode deep brain stimulation with dual targeting at dual frequency for the treatment of chronic pain: a case series and review of the literature. Brain Sci. 2017;7(1):9.
Sims-Williams HP, Javed S, Pickering AE, Patel NK. Characterising the analgesic effect of different targets for deep brain stimulation in trigeminal anaesthesia dolorosa. Stereotact Funct Neurosurg. 2016;94(3):174-181.
Kashanian A, DiCesare JAT, Rohatgi P, et al. Case series: deep brain stimulation for facial pain. Oper Neurosurg. 2020;19(5):510-517.
Kim W, Chivukula S, Hauptman J, Pouratian N. Diffusion tensor imaging-based thalamic segmentation in deep brain stimulation for chronic pain conditions. Stereotact Funct Neurosurg. 2016;94(4):225-234.
Hirato M, Miyagishima T, Gouda T, Takahashi A, Yoshimoto Y. Electrical thalamic stimulation in the anterior part of the ventral posterolateral nucleus for the treatment of patients with central poststroke pain. Neuromodulation. 2021;24(2):361-372.
Tanei T, Kajita Y, Maesawa S, et al. Long-term effect and predictive factors of motor cortex and spinal cord stimulation for chronic neuropathic pain. Neurol Med Chir. 2018;58(10):422-434.
Tanei T, Kajita Y, Noda H, et al. Efficacy of motor cortex stimulation for intractable central neuropathic pain: comparison of stimulation parameters between post-stroke pain and other central pain. Neurol Med Chir. 2011;51(1):8-14.
Abreu V, Vaz R, Chamadoira C, et al. Thalamic deep brain stimulation for post-traumatic neuropathic limb pain: efficacy at five years’ follow-up and effective volume of activated brain tissue. Neurochirurgie. 2022;68(1):52-60.
Abreu V, Vaz R, Rebelo V, et al. Thalamic deep brain stimulation for neuropathic pain: efficacy at three years’ follow-up. Neuromodulation. 2017;20(5):504-513.
Franzini A, Messina G, Levi V, et al. Deep brain stimulation of the posterior limb of the internal capsule in the treatment of central poststroke neuropathic pain of the lower limb: case series with long-term follow-up and literature review. J Neurosurg. 2019;133(3):830-383.
Levi V, Cordella R, D’Ammando A, et al. Dorsal anterior cingulate cortex (ACC) deep brain stimulation (DBS): a promising surgical option for the treatment of refractory thalamic pain syndrome (TPS). Acta Neurochir. 2019;161(8):1579-1588.
Henssen DJHA, Kurt E, van Cappellen van Walsum AM, et al. Long-term effect of motor cortex stimulation in patients suffering from chronic neuropathic pain: an observational study. PLoS One. 2018;13(1):e0191774.
Boccard SGJ, Fitzgerald JJ, Pereira EAC, et al. Targeting the affective component of chronic pain: a case series of deep brain stimulation of the anterior cingulate cortex. Neurosurgery. 2014;74(6):628-637; discussion 635-637.
Boccard SGJ, Prangnell SJ, Pycroft L, et al. Long-term results of deep brain stimulation of the anterior cingulate cortex for neuropathic pain. World Neurosurg. 2017;106:625-637.
Carroll D, Joint C, Maartens N, Shlugman D, Stein J, Aziz TZ. Motor cortex stimulation for chronic neuropathic pain: a preliminary study of 10 cases. Pain. 2000;84(2-3):431-437.
Sol JC, Casaux J, Roux FE, et al. Chronic motor cortex stimulation for phantom limb pain: correlations between pain relief and functional imaging studies. Stereotact Funct Neurosurg. 2001;77(1-4):172-176.
Sokal P, Harat M, Zieliński P, Furtak J, Paczkowski D, Rusinek M. Motor cortex stimulation in patients with chronic central pain. Adv Clin Exp Med. 2015;24(2):289-296.
Sachs AJ, Babu H, Su YF, Miller KJ, Henderson JM. Lack of efficacy of motor cortex stimulation for the treatment of neuropathic pain in 14 patients. Neuromodulation. 2014;17(4):303-311; discussion 310-311.
Buchanan RJ, Darrow D, Monsivais D, Nadasdy Z, Gjini K. Motor cortex stimulation for neuropathic pain syndromes: a case series experience. Neuroreport. 2014;25(9):715-717.
Delavallée M, Finet P, de Tourtchaninoff M, Raftopoulos C. Subdural motor cortex stimulation: feasibility, efficacy and security on a series of 18 consecutive cases with a follow-up of at least 3 years. Acta Neurochir. 2014;156(12):2289-2294.
Delavallée M, Abu-Serieh B, de Tourchaninoff M, Raftopoulos C. Subdural motor cortex stimulation for central and peripheral neuropathic pain: a long-term follow-up study in a series of eight patients. Neurosurgery. 2008;63(1):101-108; discussion 105-108.
Maarrawi J, Peyron R, Mertens P, et al. Brain opioid receptor density predicts motor cortex stimulation efficacy for chronic pain. Pain. 2013;154(11):2563-2568.
Im SH, Ha SW, Kim DR, Son BC. Long-term results of motor cortex stimulation in the treatment of chronic, intractable neuropathic pain. Stereotact Funct Neurosurg. 2015;93(3):212-218.
Slotty PJ, Eisner W, Honey CR, Wille C, Vesper J. Long-term follow-up of motor cortex stimulation for neuropathic pain in 23 patients. Stereotact Funct Neurosurg. 2015;93(3):199-205.
Hosomi K, Saitoh Y, Kishima H, et al. Electrical stimulation of primary motor cortex within the central sulcus for intractable neuropathic pain. Clin Neurophysiol. 2008;119(5):993-1001.
Ali M, Saitoh Y, Oshino S, et al. Differential efficacy of electric motor cortex stimulation and lesioning of the dorsal root entry zone for continuous vs paroxysmal pain after brachial plexus avulsion. Neurosurgery. 2011;68(5):1252-1258; discussion 1257-1258.
Saitoh Y, Hirano S, Kato A, et al. Motor cortex stimulation for deafferentation pain. Neurosurg Focus. 2001;11(3):e1.
Raghu ALB, Martin SC, Parker T, Aziz TZ, Green AL. Connectivity-based thalamus parcellation and surgical targeting of somatosensory subnuclei. J Neurosurg. 2021;137(1):209-216.
Luo H, Huang Y, Xiao X, et al. Functional dynamics of thalamic local field potentials correlate with modulation of neuropathic pain. Eur J Neurosci. 2020;51(2):628-640.
Luo H, Huang Y, Du X, et al. Dynamic neural state identification in deep brain local field potentials of neuropathic pain. Front Neurosci. 2018;12:237.
Huang Y, Green AL, Hyam J, Fitzgerald J, Aziz TZ, Wang S. Oscillatory neural representations in the sensory thalamus predict neuropathic pain relief by deep brain stimulation. Neurobiol Dis. 2018;109(Pt A):117-126.
Huang Y, Luo H, Green AL, Aziz TZ, Wang S. Characteristics of local field potentials correlate with pain relief by deep brain stimulation. Clin Neurophysiol. 2016;127(7):2573-2580.
Pereira EAC, Boccard SG, Linhares P, et al. Thalamic deep brain stimulation for neuropathic pain after amputation or brachial plexus avulsion. Neurosurg Focus. 2013;35(3):e7.
Pereira EAC, Green AL, Bradley KM, et al. Regional cerebral perfusion differences between periventricular grey, thalamic and dual target deep brain stimulation for chronic neuropathic pain. Stereotact Funct Neurosurg. 2007;85(4):175-183.
Green AL, Owen SLF, Davies P, Moir L, Aziz TZ. Deep brain stimulation for neuropathic cephalalgia. Cephalalgia. 2006;26(5):561-567.
Owen SLF, Green AL, Nandi D, Bittar RG, Wang S, Aziz TZ. Deep brain stimulation for neuropathic pain. Neuromodulation. 2006;9(2):100-106.
Owen SLF, Green AL, Stein JF, Aziz TZ. Deep brain stimulation for the alleviation of post-stroke neuropathic pain. Pain. 2006;120(1-2):202-206.
Bittar RG, Otero S, Carter H, Aziz TZ. Deep brain stimulation for phantom limb pain. J Clin Neurosci. 2005;12(4):399-404.
Green AL, Shad A, Watson R, Nandi D, Yianni J, Aziz TZ. N-of-1 trials for assessing the efficacy of deep brain stimulation in neuropathic pain. Neuromodulation. 2004;7(2):76-81.
Nandi D, Aziz T, Carter H, Stein J. Thalamic field potentials in chronic central pain treated by periventricular gray stimulation -- a series of eight cases. Pain. 2003;101(1-2):97-107.
Nandi D, Smith H, Owen S, Joint C, Stein J, Aziz T. Peri-ventricular grey stimulation versus motor cortex stimulation for post stroke neuropathic pain. J Clin Neurosci. 2002;9(5):557-561.
Polanski WH, Zolal A, Klein J, et al. Somatosensory functional MRI tractography for individualized targeting of deep brain stimulation in patients with chronic pain after brachial plexus injury. Acta Neurochir. 2019;161(12):2485-2490.
Raslan AM, Nasseri M, Bahgat D, Abdu E, Burchiel KJ. Motor cortex stimulation for trigeminal neuropathic or deafferentation pain: an institutional case series experience. Stereotact Funct Neurosurg. 2011;89(2):83-88.
Gray AM, Pounds-Cornish E, Eccles FJR, Aziz TZ, Green AL, Scott RB. Deep brain stimulation as a treatment for neuropathic pain: a longitudinal study addressing neuropsychological outcomes. J Pain. 2014;15(3):283-292.
Staudt MD, Clark AJ, Gordon AS, et al. Long-term outcomes in the management of central neuropathic pain syndromes: a prospective observational cohort study. Can J Neurol Sci. 2018;45(5):545-552.
Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron. 2006;52(1):77-92.
Lempka SF, Malone DA Jr, Hu B, et al. Randomized clinical trial of deep brain stimulation for poststroke pain. Ann Neurol. 2017;81(5):653-663.
Shirvalkar P, Sellers KK, Schmitgen A, et al. A deep brain stimulation trial period for treating chronic pain. J Clin Med. 2020;9(10):3155.