The effect of Virtual Reality on evoked potentials following painful electrical stimuli and subjective pain

E J Lier, J M Oosterman, R Assmann, M de Vries, H van Goor, E J Lier, J M Oosterman, R Assmann, M de Vries, H van Goor

Abstract

Background: Virtual reality (VR) has been shown to reduce pain, however outcome parameters of previous studies have primarily been of a subjective nature and susceptible to bias. This study investigated the effect of VR on cortical processing of evoked potentials (EPs) and subjectively reported pain. Additionally, we explored whether subjects' demographic and personal characteristics modulated the effect of VR analgesia.

Methods: Three VR conditions were compared in a randomized cross-over study of 30 healthy volunteers: Passive VR (i.e. no interaction possible with the virtual world), active VR (interactive virtual environment) and no VR (black screen). Subjects received noxious electrical stimuli at random intervals during all conditions. EPs, recorded at Cz, were extracted time locked to stimuli. Pain scores were reported after each condition.

Results: Active VR significantly decreased pain scores and amplitudes of N1 and P3. Passive VR had no analgesic effect. Age was significantly correlated to pain scores, with older subjects demonstrating larger effects of VR. Gender, game experience, and susceptibility for immersion, did not influence VR analgesia.

Conclusion: Active VR decreases pre-perceptual and perceptual brain activity following painful electrical stimuli, corresponding with reduced pain experience. VR has potential to serve as a non-pharmacologic treatment for pain, particularly in elderly patients.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Screenshots of the Virtual Reality conditions: (a) control condition, (b) passive condition, (c) active condition.
Figure 2
Figure 2
(a) Grand average N1 and P3 peaks during active VR, passive VR and the control condition. (b) Brain activity topography at 130 ms during each condition. (c) Brain activity topography at 238 ms during each condition.
Figure 3
Figure 3
Individual N1 (a) and P3 (b) amplitudes during each condition.
Figure 4
Figure 4
Individual pain scores (NRS) during each condition.

References

    1. Sinatra R. Causes and consequences of inadequate management of acute pain. Pain. Med. 2010;11:1859–1871. doi: 10.1111/j.1526-4637.2010.00983.x.
    1. Gan TJ, Habib AS, Miller TE, White W, Apfelbaum JL. Incidence, patient satisfaction, and perceptions of post-surgical pain: results from a US national survey. Curr. Med. Res. Opin. 2014;30:149–160. doi: 10.1185/03007995.2013.860019.
    1. Benyamin R, et al. Opioid complications and side effects. Pain. Physician. 2008;11:S105–120.
    1. Sostres C, Gargallo CJ, Arroyo MT, Lanas A. Adverse effects of non-steroidal anti-inflammatory drugs (NSAIDs, aspirin and coxibs) on upper gastrointestinal tract. Best. Pract. Res. Clin. Gastroenterol. 2010;24:121–132. doi: 10.1016/j.bpg.2009.11.005.
    1. Scheffler M, Koranyi S, Meissner W, Strauss B, Rosendahl J. Efficacy of non-pharmacological interventions for procedural pain relief in adults undergoing burn wound care: A systematic review and meta-analysis of randomized controlled trials. Burns. 2018;44:1709–1720. doi: 10.1016/j.burns.2017.11.019.
    1. Hoffman H. G. et al. In Virtual Reality for Psychological and Neurocognitive Interventions (ed Bouchard S. Rizzo A.) Ch. 8, 195–208 (Springer Nature, 2019).
    1. McCaul KD, Malott JM. Distraction and coping with pain. Psychol. Bull. 1984;95:516–533. doi: 10.1037/0033-2909.95.3.516.
    1. Melzack R, Wall PD. Pain mechanisms: a new theory. Science. 1965;150:971–979. doi: 10.1126/science.150.3699.971.
    1. Triberti S, Repetto C, Riva G. Psychological factors influencing the effectiveness of virtual reality-based analgesia: a systematic review. Cyberpsychol Behav. Soc. Netw. 2014;17:335–345. doi: 10.1089/cyber.2014.0054.
    1. Hoffman HG, Doctor JN, Patterson DR, Carrougher GJ, Furness TA., III. Virtual reality as an adjunctive pain control during burn wound care in adolescent patients. Pain. 2000;85:305–309. doi: 10.1016/s0304-3959(99)00275-4.
    1. Gutierrez-Maldonado J, Gutierrez-Martinez O, Cabas-Hoyos K. Interactive and passive virtual reality distraction: effects on presence and pain intensity. Stud. Health Technol. Inf. 2011;167:69–73.
    1. Alshatrat, S. M., Alotaibi, R., Sirois, M. & Malkawi, Z. The use of immersive virtual reality for pain control during periodontal scaling and root planing procedures in dental hygiene clinic. Int J Dent Hyg (2018).
    1. Piskorz, J. & Czub, M. Effectiveness of a virtual reality intervention to minimize pediatric stress and pain intensity during venipuncture. Journal for specialists in pediatric nursing: JSPN23 (2018).
    1. Chan E, Foster S, Sambell R, Leong P. Clinical efficacy of virtual reality for acute procedural pain management: A systematic review and meta-analysis. Plos one. 2018;13:e0200987. doi: 10.1371/journal.pone.0200987.
    1. Luo H, Cao C, Zhong J, Chen J, Cen Y. Adjunctive virtual reality for procedural pain management of burn patients during dressing change or physical therapy: A systematic review and meta-analysis of randomized controlled trials. Wound Repair. Regen. 2019;27:90–101. doi: 10.1111/wrr.1.
    1. Malloy KM, Milling LS. The effectiveness of virtual reality distraction for pain reduction: a systematic review. Clin. Psychol. Rev. 2010;30:1011–1018. doi: 10.1016/j.cpr.2010.07.001.
    1. Mosso-Vazquez JL, Gao K, Wiederhold BK, Wiederhold MD. Virtual reality for pain management in cardiac surgery. Cyberpsychol Behav. Soc. Netw. 2014;17:371–378. doi: 10.1089/cyber.2014.0198.
    1. Tashjian VC, et al. Virtual Reality for Management of Pain in Hospitalized Patients: Results of a Controlled Trial. JMIR Ment. Health. 2017;4:e9. doi: 10.2196/mental.7387.
    1. Jones T, Moore T, Choo J. The Impact of Virtual Reality on Chronic Pain. Plos one. 2016;11:e0167523. doi: 10.1371/journal.pone.0167523.
    1. Demeter N, Josman N, Eisenberg E, Pud D. Who can benefit from virtual reality to reduce experimental pain? A crossover study in healthy subjects. Eur. J. pain. 2015;19:1467–1475. doi: 10.1002/ejp.678.
    1. Magora F, Cohen S, Shochina M, Dayan E. Virtual reality immersion method of distraction to control experimental ischemic pain. Isr. Med. Assoc. J. 2006;8:261–265.
    1. Wood L, et al. Empirical evidence of bias in treatment effect estimates in controlled trials with different interventions and outcomes: meta-epidemiological study. BMJ. 2008;336:601–605. doi: 10.1136/.
    1. Boutron I, et al. CONSORT Statement for Randomized Trials of Nonpharmacologic Treatments: A 2017 Update and a CONSORT Extension for Nonpharmacologic Trial Abstracts. Ann. Intern. Med. 2017;167:40–47. doi: 10.7326/M17-0046.
    1. Hoffman Hunter G., Richards Todd L., Van Oostrom Trevor, Coda Barbara A., Jensen Mark P., Blough David K., Sharar Sam R. The Analgesic Effects of Opioids and Immersive Virtual Reality Distraction: Evidence from Subjective and Functional Brain Imaging Assessments. Anesthesia & Analgesia. 2007;105(6):1776–1783. doi: 10.1213/01.ane.0000270205.45146.db.
    1. Wiederhold BK, Gao K, Sulea C, Wiederhold MD. Virtual reality as a distraction technique in chronic pain patients. Cyberpsychol Behav. Soc. Netw. 2014;17:346–352. doi: 10.1089/cyber.2014.0207.
    1. Hoffman HG, et al. Modulation of thermal pain-related brain activity with virtual reality: evidence from fMRI. Neuroreport. 2004;15:1245–1248. doi: 10.1097/01.wnr.0000127826.73576.91.
    1. Luck, S. J. An introduction to the event-related potential technique. (MIT, 2005).
    1. Lee MC, Mouraux A, Iannetti GD. Characterizing the cortical activity through which pain emerges from nociception. J. neuroscience: Off. J. Soc. Neurosci. 2009;29:7909–7916. doi: 10.1523/JNEUROSCI.0014-09.2009.
    1. Garcia-Larrea L, Peyron R, Laurent B, Mauguiere F. Association and dissociation between laser-evoked potentials and pain perception. Neuroreport. 1997;8:3785–3789. doi: 10.1097/00001756-199712010-00026.
    1. Picton, T. W. Human event-related potentials. (Elsevier, 1988).
    1. Wender R, et al. Interactivity Influences the Magnitude of Virtual Reality Analgesia. J. Cyber Ther. Rehabil. 2009;2:27–33.
    1. Dahlquist LM, et al. Active and passive distraction using a head-mounted display helmet: effects on cold pressor pain in children. Health Psychol. 2007;26:794–801. doi: 10.1037/0278-6133.26.6.794.
    1. Lier EJ, Harder J, Oosterman JM, de Vries M, van Goor H. Modulation of tactile perception by Virtual Reality distraction: The role of individual and VR-related factors. Plos one. 2018;13:e0208405. doi: 10.1371/journal.pone.0208405.
    1. Schubert T. The sense of presence in virtual environments: A three-component scale measuring spatial presence, involvement, and realness. Z. für Medienpsychologie. 2003;15:69–71. doi: 10.1026//1617-6383.15.2.69.
    1. Katsarava Z, et al. A novel method of eliciting pain-related potentials by transcutaneous electrical stimulation. Headache. 2006;46:1511–1517. doi: 10.1111/j.1526-4610.2006.00446.x.
    1. Klem GH, Luders HO, Jasper HH, Elger C. The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. Electroencephalogr. Clin. Neurophysiol. Suppl. 1999;52:3–6.
    1. Gratton G, Coles MG, Donchin E. A new method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 1983;55:468–484. doi: 10.1016/0013-4694(83)90135-9.
    1. Ab Aziz CB, Ahmad AH. The role of the thalamus in modulating pain. Malays. J. Med. Sci. 2006;13:11–18.
    1. Legrain V, Guerit JM, Bruyer R, Plaghki L. Attentional modulation of the nociceptive processing into the human brain: selective spatial attention, probability of stimulus occurrence, and target detection effects on laser evoked potentials. Pain. 2002;99:21–39. doi: 10.1016/S0304-3959(02)00051-9.
    1. Mouraux A, Iannetti GD. Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J. Neurophysiol. 2009;101:3258–3269. doi: 10.1152/jn.91181.2008.
    1. Dahlquist LM, et al. Effects of videogame distraction using a virtual reality type head-mounted display helmet on cold pressor pain in children. J. Pediatr. Psychol. 2009;34:574–584. doi: 10.1093/jpepsy/jsn023.
    1. Hoffman HG, et al. Virtual reality helmet display quality influences the magnitude of virtual reality analgesia. J. Pain. 2006;7:843–850. doi: 10.1016/j.jpain.2006.04.006.
    1. de Tommaso M, et al. Virtual visual effect of hospital waiting room on pain modulation in healthy subjects and patients with chronic migraine. Pain. Res. Treat. 2013;2013:515730. doi: 10.1155/2013/515730.
    1. Mullinger K, Bowtell R. Combining EEG and fMRI. Methods Mol. Biol. 2011;711:303–326. doi: 10.1007/978-1-61737-992-5_15.
    1. Indovina P, et al. Virtual Reality as a Distraction Intervention to Relieve Pain and Distress During Medical Procedures: A Comprehensive Literature Review. Clin. J. Pain. 2018;34:858–877. doi: 10.1097/ajp.0000000000000599.
    1. Kaye AD, Baluch A, Scott JT. Pain management in the elderly population: a review. Ochsner J. 2010;10:179–187.
    1. Huygelier H, Schraepen B, van Ee R, Vanden Abeele V, Gillebert CR. Acceptance of immersive head-mounted virtual reality in older adults. Sci. Rep. 2019;9:4519. doi: 10.1038/s41598-019-41200-6.

Source: PubMed

3
Prenumerera