Brain-computer interface relieves chronic chemotherapy-induced peripheral neuropathy: A randomized, double-blind, placebo-controlled trial.
brain-computer interface
electroencephalograph (EEG)
neuromodulation
neuropathy
pain
placebo
Journal
Cancer
ISSN: 1097-0142
Titre abrégé: Cancer
Pays: United States
ID NLM: 0374236
Informations de publication
Date de publication:
21 Sep 2023
21 Sep 2023
Historique:
revised:
20
07
2023
received:
11
11
2022
accepted:
27
07
2023
medline:
21
9
2023
pubmed:
21
9
2023
entrez:
21
9
2023
Statut:
aheadofprint
Résumé
Chemotherapy-induced peripheral neuropathy (CIPN) includes negative sensations that remain a major chronic problem for cancer survivors. Previous research demonstrated that neurofeedback (a closed-loop brain-computer interface [BCI]) was effective at treating CIPN versus a waitlist control (WLC). The authors' a priori hypothesis was that BCI would be superior to placebo feedback (placebo control [PLC]) and to WLC in alleviating CIPN and that changes in brain activity would predict symptom report. Randomization to one of three conditions occurred between November 2014 and November 2018. Breast cancer survivors no longer in treatment were assessed at baseline, at the end of 20 treatment sessions, and 1 month later. Auditory and visual rewards were given over 20 sessions based on each patient's ability to modify their own electroencephalographic signals. The Pain Quality Assessment Scale (PQAS) at the end of treatment was the primary outcome, and changes in electroencephalographic signals and 1-month data also were examined. The BCI and PLC groups reported significant symptom reduction. The BCI group demonstrated larger effect size differences from the WLC group than the PLC group (mean change score: BCI vs. WLC, -2.60 vs. 0.38; 95% confidence interval, -3.67, -1.46 [p = .000; effect size, 1.07]; PLC, -2.26; 95% confidence interval, -3.33, -1.19 [p = .001 vs. WLC; effect size, 0.9]). At 1 month, symptoms continued to improve only for the BCI group. Targeted brain changes at the end of treatment predicted symptoms at 1 month for the BCI group only. BCI is a promising treatment for CIPN and may have a longer lasting effect than placebo (nonspecific BCI), which is an important consideration for long-term symptom relief. Although scientifically interesting, the ability to separate real from placebo treatment may not be as important as understanding the placebo effects differently from effects of the intervention. Chemotherapy-induced nerve pain (neuropathy) can be disabling for cancer survivors; however, the way symptoms are felt depends on how the brain interprets the signals from nerves in the body. We determined that the perception of neuropathy can be changed by working directly with the brain. Survivors in our trial played 20 sessions of a type of video game that was designed to change the way the brain processed sensation and movement. In this, our second trial, we again observed significant improvement in symptoms that lasted after the treatment was complete.
Sections du résumé
BACKGROUND
BACKGROUND
Chemotherapy-induced peripheral neuropathy (CIPN) includes negative sensations that remain a major chronic problem for cancer survivors. Previous research demonstrated that neurofeedback (a closed-loop brain-computer interface [BCI]) was effective at treating CIPN versus a waitlist control (WLC). The authors' a priori hypothesis was that BCI would be superior to placebo feedback (placebo control [PLC]) and to WLC in alleviating CIPN and that changes in brain activity would predict symptom report.
METHODS
METHODS
Randomization to one of three conditions occurred between November 2014 and November 2018. Breast cancer survivors no longer in treatment were assessed at baseline, at the end of 20 treatment sessions, and 1 month later. Auditory and visual rewards were given over 20 sessions based on each patient's ability to modify their own electroencephalographic signals. The Pain Quality Assessment Scale (PQAS) at the end of treatment was the primary outcome, and changes in electroencephalographic signals and 1-month data also were examined.
RESULTS
RESULTS
The BCI and PLC groups reported significant symptom reduction. The BCI group demonstrated larger effect size differences from the WLC group than the PLC group (mean change score: BCI vs. WLC, -2.60 vs. 0.38; 95% confidence interval, -3.67, -1.46 [p = .000; effect size, 1.07]; PLC, -2.26; 95% confidence interval, -3.33, -1.19 [p = .001 vs. WLC; effect size, 0.9]). At 1 month, symptoms continued to improve only for the BCI group. Targeted brain changes at the end of treatment predicted symptoms at 1 month for the BCI group only.
CONCLUSIONS
CONCLUSIONS
BCI is a promising treatment for CIPN and may have a longer lasting effect than placebo (nonspecific BCI), which is an important consideration for long-term symptom relief. Although scientifically interesting, the ability to separate real from placebo treatment may not be as important as understanding the placebo effects differently from effects of the intervention.
PLAIN LANGUAGE SUMMARY
CONCLUSIONS
Chemotherapy-induced nerve pain (neuropathy) can be disabling for cancer survivors; however, the way symptoms are felt depends on how the brain interprets the signals from nerves in the body. We determined that the perception of neuropathy can be changed by working directly with the brain. Survivors in our trial played 20 sessions of a type of video game that was designed to change the way the brain processed sensation and movement. In this, our second trial, we again observed significant improvement in symptoms that lasted after the treatment was complete.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Center for Complimentary and Integrative Health
ID : 1K01AT008485-01
Organisme : The Rising Tide Foundation
ID : CCR-14-800
Informations de copyright
© 2023 American Cancer Society.
Références
Majithia N, Loprinzi CL, Smith TJ. New practical approaches to chemotherapy-induced neuropathic pain: prevention, assessment, and treatment. Oncology (Williston Park). 2016;30(11):1020-1029.
Hershman DL, Weimer LH, Wang A, et al. Association between patient reported outcomes and quantitative sensory tests for measuring long-term neurotoxicity in breast cancer survivors treated with adjuvant paclitaxel chemotherapy. Breast Cancer Res Treat. 2011;125(3):767-774. doi:10.1007/s10549-010-1278-0
Majithia N, Temkin SM, Ruddy KJ, Beutler AS, Hershman DL, Loprinzi CL. National Cancer Institute-supported chemotherapy-induced peripheral neuropathy trials: outcomes and lessons. Support Care Cancer. 2016;24(3):1439-1447. doi:10.1007/s00520-015-3063-4
Prinsloo S, Novy D, Driver L, et al. The long-term impact of neurofeedback on symptom burden and interference in patients with chronic chemotherapy-induced neuropathy: analysis of a randomized controlled trial. J Pain Symptom Manag. 2018;55(5):1276-1285. doi:10.1016/j.jpainsymman.2018.01.010
Prinsloo S, Novy D, Driver L, et al. Randomized controlled trial of neurofeedback on chemotherapy-induced peripheral neuropathy: a pilot study. Cancer. 2017;123(11):1989-1997. doi:10.1002/cncr.30649
Kjaer SW, Rice ASC, Wartolowska K, Vase L. Neuromodulation: more than a placebo effect? Pain. 2020;161(3):491-495. doi:10.1097/j.pain.0000000000001727
Kaptchuk TJ, Miller FG. Placebo effects in medicine. N Engl J Med. 2015;373(1):8-9. doi:10.1056/nejmp1504023
Enblom A, Johnsson A, Hammar M, Onelov E, Steineck G, Borjeson S. Acupuncture compared with placebo acupuncture in radiotherapy-induced nausea-a randomized controlled study. Ann Oncol. 2012;23(5):1353-1361. doi:10.1093/annonc/mdr402
Kaptchuk TJ, Kelley JM, Conboy LA, et al. Components of placebo effect: randomised controlled trial in patients with irritable bowel syndrome. BMJ. 2008;336(7651):999-1003. doi:10.1136/bmj.39524.439618.25
Holtedahl R, Brox JI, Tjomsland O. Placebo effects in trials evaluating 12 selected minimally invasive interventions: a systematic review and meta-analysis. BMJ Open. 2015;5(1):e007331. doi:10.1136/bmjopen-2014-007331
Wartolowska KA, Feakins BG, Collins GS, et al. The magnitude and temporal changes of response in the placebo arm of surgical randomized controlled trials: a systematic review and meta-analysis. Trials. 2016;17(1):589. doi:10.1186/s13063-016-1720-7
Jonas WB, Crawford C, Colloca L, et al. Are invasive procedures effective for chronic pain? A systematic review. Pain Med. 2019;20(7):1281-1293. doi:10.1093/pm/pny154
Smith EM, Pang H, Cirrincione C, et al. Effect of duloxetine on pain, function, and quality of life among patients with chemotherapy-induced painful peripheral neuropathy: a randomized clinical trial. JAMA. 2013;309(13):1359-1367. doi:10.1001/jama.2013.2813
Younger J, McCue R, Mackey S. Pain outcomes: a brief review of instruments and techniques. Curr Pain Headache Rep. 2009;13(1):39-43. doi:10.1007/s11916-009-0009-x
Besen E, Gaines B, Linton LJ, Shaw WS. The role of pain catastrophizing as a mediator in the work disability process following acute low back pain. J Appl Biobehav Res. 2017;22(1):e12085. doi:10.1111/jabr.12085
Kovacs FM, Seco J, Royuela A, Pena A, Muriel A; Spanish Back Pain Research Network. The correlation between pain, catastrophizing, and disability in subacute and chronic low back pain: a study in the routine clinical practice of the Spanish National Health Service. Spine (Phila Pa 1976). 2011;36(4):339-345. doi:10.1097/brs.0b013e3181cfba29
Garbi MdO, Hortense P, Gomez RR, da Silva Tde C, Castanho AC, Sousa FA. Pain intensity, disability and depression in individuals with chronic back pain. Rev Lat Am Enfermagem. 2014;22(4):569-575. doi:10.1590/0104-1169.3492.2453
Mulert C, Jager L, Schmitt R, et al. Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage. 2004;22(1):83-94. doi:10.1016/j.neuroimage.2003.10.051
Thatcher RW, North DM, Biver CJ. Diffusion spectral imaging modules correlate with EEG LORETA neuroimaging modules. Hum Brain Mapp. 2012;33(5):1062-1075. doi:10.1002/hbm.21271
Congedo M, Lubar JF, Joffe D. Low-resolution electromagnetic tomography neurofeedback. IEEE Trans Neural Syst Rehabil Eng. 2004;12(4):387-397. doi:10.1109/tnsre.2004.840492
Field A. Discovering Statistics Using IBM SPSS Statistics. 4th ed. Sage Publications Ltd.; 2013.
Rowbotham MC. What is a “clinically meaningful” reduction in pain? Pain. 2001;94(2):131-132. doi:10.1016/s0304-3959(01)00371-2
Maeda Y, Kim H, Kettner N, et al. Rewiring the primary somatosensory cortex in carpal tunnel syndrome with acupuncture. Brain. 2017;140(4):914-927. doi:10.1093/brain/awx015
Sarnthein J, Stern J, Aufenberg C, Rousson V, Jeanmonod D. Increased EEG power and slowed dominant frequency in patients with neurogenic pain. Brain. 2006;129(pt 1):55-64. doi:10.1093/brain/awh631
Stern J, Jeanmonod D, Sarnthein J. Persistent EEG overactivation in the cortical pain matrix of neurogenic pain patients. Neuroimage. 2006;31(2):721-731. doi:10.1016/j.neuroimage.2005.12.042
Boord P, Siddall PJ, Tran Y, Herbert D, Middleton J, Craig A. Electroencephalographic slowing and reduced reactivity in neuropathic pain following spinal cord injury. Spinal Cord. 2008;46(2):118-123. doi:10.1038/sj.sc.3102077
Finniss DG, Kaptchuk TJ, Miller F, Benedetti F. Biological, clinical, and ethical advances of placebo effects. Lancet. 2010;375(9715):686-695. doi:10.1016/s0140-6736(09)61706-2
Meissner K, Bingel U, Colloca L, Wager TD, Watson A, Flaten MA. The placebo effect: advances from different methodological approaches. J Neurosci. 2011;31(45):16117-16124. doi:10.1523/jneurosci.4099-11.2011
Colloca L, Benedetti F. How prior experience shapes placebo analgesia. Pain. 2006;124(1-2):126-133. doi:10.1016/j.pain.2006.04.005
Meissner K, Fassler M, Rucker G, et al. Differential effectiveness of placebo treatments: a systematic review of migraine prophylaxis. JAMA Intern Med. 2013;173(21):1941-1951. doi:10.1001/jamainternmed.2013.10391
Kaptchuk TJ, Goldman P, Stone DA, Stason WB. Do medical devices have enhanced placebo effects? J Clin Epidemiol. 2000;53(8):786-792. doi:10.1016/s0895-4356(00)00206-7
Wager TD, Rilling JK, Smith EE, et al. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science. 2004;303(5661):1162-1167. doi:10.1126/science.1093065