Effects of chiropractic spinal manipulation on laser-evoked pain and brain activity

Benjamin Provencher, Stéphane Northon, Carlos Gevers Montoro, Julie O'Shaughnessy, Mathieu Piché, Benjamin Provencher, Stéphane Northon, Carlos Gevers Montoro, Julie O'Shaughnessy, Mathieu Piché

Abstract

The aim of this study was to examine the mechanisms underlying hypoalgesia induced by spinal manipulation (SM). Eighty-two healthy volunteers were assigned to one of the four intervention groups: no intervention, SM at T4 (homosegmental to pain), SM at T8 (heterosegmental to pain) or light mechanical stimulus at T4 (placebo). Eighty laser stimuli were applied on back skin at T4 to evoke pain and brain activity related to Aδ- and C-fibers activation. The intervention was performed after 40 stimuli. Laser pain was decreased by SM at T4 (p = 0.028) but not T8 (p = 0.13), compared with placebo. However, brain activity related to Aδ-fibers activation was not significantly modulated (all p > 0.05), while C-fiber activity could not be measured reliably. This indicates that SM produces segmental hypoalgesia through inhibition of nociceptive processes that are independent of Aδ fibers. It remains to be clarified whether the effect is mediated by the inhibition of C-fiber activity.

Keywords: Electroencephalography; Hypoalgesia; Nociceptive fibers; Spinal manipulation.

References

    1. Arendt-Nielsen L (2015) Central sensitization in humans: assessment and pharmacology. Handb Exp Pharmacol 227:79–102.
    1. Aspinall SL, Jacques A, Leboeuf-Yde C, Etherington SJ, Walker BF (2019) No difference in pressure pain threshold and temporal summation after lumbar spinal manipulation compared to sham: a randomised controlled trial in adults with low back pain. Musculoskelet Sci Pract 43:18–25.
    1. Babiloni C, Babiloni F, Carducci F, Cincotti F, Rosciarelli F, Arendt-Nielsen L, Chen AC, Rossini PM (2002) Human brain oscillatory activity phase-locked to painful electrical stimulations: a multi-channel EEG study. Hum Brain Mapp 15(2):112–123.
    1. Bialosky JE, Beneciuk JM, Bishop MD, Coronado RA, Penza CW, Simon CB, George SZ (2018) Unraveling the mechanisms of manual therapy: modeling an approach. J Orthop Sports Phys Ther 48(1):8–18.
    1. Bialosky JE, Bishop MD, Penza CW (2017) Placebo mechanisms of manual therapy: a sheep in wolf’s clothing? J Orthop Sports Phys Ther 47(5):301–304.
    1. Bialosky JE, Bishop MD, Robinson ME, Barabas JA, George SZ (2008) The influence of expectation on spinal manipulation induced hypoalgesia: an experimental study in normal subjects. BMC Musculoskelet Disord 9:19.
    1. Bialosky JE, Bishop MD, Robinson ME, Zeppieri G Jr, George SZ (2009) Spinal manipulative therapy has an immediate effect on thermal pain sensitivity in people with low back pain: a randomized controlled trial. Phys Ther 89(12):1292–1303.
    1. Bialosky JE, George SZ, Horn ME, Price DD, Staud R, Robinson ME (2014) Spinal manipulative therapy-specific changes in pain sensitivity in individuals with low back pain (NCT01168999). J Pain 15(2):136–148.
    1. Bishop MD, Beneciuk JM, George SZ (2011) Immediate reduction in temporal sensory summation after thoracic spinal manipulation. Spine J 11(5):440–446.
    1. Bishop MD, Bialosky JE, Penza CW, Beneciuk JM, Alappattu MJ (2017) The influence of clinical equipoise and patient preferences on outcomes of conservative manual interventions for spinal pain: an experimental study. J Pain Res 10:965–972.
    1. Bromm B, Jahnke MT, Treede RD (1984) Responses of human cutaneous afferents to CO2 laser stimuli causing pain. Exp Brain Res 55(1):158–166.
    1. Bussières AE, Stewart G, Al-Zoubi F, Decina P, Descarreaux M, Haskett D, Hincapié C, Pagé I, Passmore S, Srbely J, Stupar M (2018) Spinal manipulative therapy and other conservative treatments for low back pain: a guideline from the canadian chiropractic guideline initiative. J Manipulative Physiol Ther 41(4):265–293.
    1. Côté P, Wong JJ, Sutton D, Shearer HM, Mior S, Randhawa K, Ameis A, Carroll LJ, Nordin M, Yu H, Lindsay GM (2016) Management of neck pain and associated disorders: a clinical practice guideline from the Ontario Protocol for Traffic Injury Management (OPTIMa) Collaboration. Eur Spine J 25(7):2000–2022.
    1. Cousineau D (2005) Confidence intervals in within-subject designs: a simpler solution to Loftus and Masson’s method. TQMP 1(1):42–45.
    1. Croft RJ, Williams JD, Haenschel C, Gruzelier JH (2002) Pain perception, hypnosis and 40 Hz oscillations. Int J Psychophysiol 46(2):101–108.
    1. Cruccu G, Iannetti GD, Agostino R, Romaniello A, Truini A, Manfredi M (2000) Conduction velocity of the human spinothalamic tract as assessed by laser evoked potentials. NeuroReport 11(13):3029–3032.
    1. Deldar Z, Rustamov N, Blanchette I, Piche M (2019) Improving working memory and pain inhibition in older persons using transcranial direct current stimulation. Neurosci Res 148:19–27.
    1. Deldar Z, Rustamov N, Bois S, Blanchette I, Piche M (2018) Enhancement of pain inhibition by working memory with anodal transcranial direct current stimulation of the left dorsolateral prefrontal cortex. J Physiol Sci 68(6):825–836.
    1. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21.
    1. Domnick C, Hauck M, Casey KL, Engel AK, Lorenz J (2009) C-fiber-related EEG-oscillations induced by laser radiant heat stimulation of capsaicin-treated skin. J Pain Res 2:49–56.
    1. Foster NE, Anema JR, Cherkin D, Chou R, Cohen SP, Gross DP, Ferreira PH, Fritz JM, Koes BW, Peul W, Turner JA (2018) Prevention and treatment of low back pain: evidence, challenges, and promising directions. The Lancet 391(10137):2368–2383.
    1. Franz M, Ritter A, Puta C, Nötzel D, Miltner WH, Weiss T (2014) Laser heat hyperalgesia is not a feature of non-specific chronic low back pain. Eur J Pain 18(10):1501–1508.
    1. Gál J, Herzog W, Kawchuk G, Conway PJ, Zhang YT (1997) Movements of vertebrae during manipulative thrusts to unembalmed human cadavers. J Manipulative Physiol Ther 20(1):30–40
    1. Garcia-Larrea L, Frot M, Valeriani M (2003) Brain generators of laser-evoked potentials: from dipoles to functional significance. Neurophysiol Clin 33(6):279–292.
    1. George SZ, Bishop MD, Bialosky JE, Zeppieri G Jr, Robinson ME (2006) Immediate effects of spinal manipulation on thermal pain sensitivity: an experimental study. BMC Musculoskelet Disord 7:68–78.
    1. Goffaux P, Redmond WJ, Rainville P, Marchand S (2007) Descending analgesia–when the spine echoes what the brain expects. Pain 130(1–2):137–143.
    1. Gyer G, Michael J, Inklebarger J, Tedla JS (2019) Spinal manipulation therapy: Is it all about the brain? A current review of the neurophysiological effects of manipulation. J Integr Med 17(5):328–337.
    1. Heid C, Mouraux A, Treede RD, Schuh-Hofer S, Rupp A, Baumgartner U (2020) Early gamma-oscillations as correlate of localized nociceptive processing in primary sensorimotor cortex. J Neurophysiol 123(5):1711–1726.
    1. Herrero JF, Laird JM, Lopez-Garcia JA (2000) Wind-up of spinal cord neurones and pain sensation: much ado about something? Prog Neurobiol 61(2):169–203.
    1. Herzog W (2010) The biomechanics of spinal manipulation. J Bodyw Mov Ther 14(3):280–286.
    1. Hu L, Cai MM, Xiao P, Luo F, Iannetti GD (2014) Human brain responses to concomitant stimulation of Adelta and C nociceptors. J Neurosci 34(34):11439–11451.
    1. Hu L, Peng W, Valentini E, Zhang Z, Hu Y (2013) Functional features of nociceptive-induced suppression of alpha band electroencephalographic oscillations. J Pain 14(1):89–99.
    1. Iannetti GD, Hughes NP, Lee MC, Mouraux A (2008) Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? J Neurophysiol 100(2):815–828.
    1. Iannetti GD, Truini A, Romaniello A, Galeotti F, Rizzo C, Manfredi M, Cruccu G (2003) Evidence of a specific spinal pathway for the sense of warmth in humans. J Neurophysiol 89(1):562–570.
    1. James SL, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, Abbastabar H, Abd-Allah F, Abdela J, Abdelalim A, Abdollahpour I (2018) Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392(10159):1789–1858.
    1. Jankovski A, Plaghki L, Mouraux A (2013) Reliable EEG responses to the selective activation of C-fibre afferents using a temperature-controlled infrared laser stimulator in conjunction with an adaptive staircase algorithm. Pain 154(9):1578–1587.
    1. Kjaer P, Kongsted A, Hartvigsen J, Isenberg-Jørgensen A, Schiøttz-Christensen B, Søborg B, Krog C, Møller CM, Halling CM, Lauridsen HH, Hansen IR (2017) National clinical guidelines for non-surgical treatment of patients with recent onset neck pain or cervical radiculopathy. Eur Spine J 26(9):2242–2257.
    1. Legrain V, Crombez G, Plaghki L, Mouraux A (2013) Shielding cognition from nociception with working memory. Cortex 49(7):1922–1934.
    1. Luck SJ (2014) An introduction to the event-related potential technique, 2nd edn. The MIT Press, Cambridge
    1. Madden VJ, Catley MJ, Grabherr L, Mazzola F, Shohag M, Moseley GL (2016) The effect of repeated laser stimuli to ink-marked skin on skin temperature-recommendations for a safe experimental protocol in humans. PeerJ 4:e1577.
    1. Mancini F, Bauleo A, Cole J, Lui F, Porro CA, Haggard P, Iannetti GD (2014) Whole-body mapping of spatial acuity for pain and touch. Ann Neurol 75(6):917–924.
    1. Millan M, Leboeuf-Yde C, Budgell B, Amorim MA (2012) The effect of spinal manipulative therapy on experimentally induced pain: a systematic literature review. Chiropr Man Therap 20(1):26.
    1. Moayedi M, Stefano G, Stubbs M, Djeugam BL, M, & Iannetti, G. (2016) Nociceptive-evoked potentials are sensitive to behaviorally relevant stimulus displacements in egocentric coordinates. ENeuro 3(3):e0151–e0163.
    1. Mouraux A, Guérit JM, Plaghki L (2003) Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between A∂- and C-fibre afferent volleys. Clin Neurophysiol 114(4):710–722.
    1. Mouraux A, Iannetti GD (2008) Across-trial averaging of event-related EEG responses and beyond. Magn Reson Imaging 26(7):1041–1054.
    1. Mouraux A, Iannetti GD (2009) Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J Neurophysiol 101(6):3258–3269.
    1. Navid MS, Lelic D, Niazi IK, Holt K, Mark EB, Drewes AM, Haavik H (2019) The effects of chiropractic spinal manipulation on central processing of tonic pain - a pilot study using standardized low-resolution brain electromagnetic tomography (sLORETA). Sci Rep 9(1):6925.
    1. Northon S, Rustamov N, Piché M (2019) Cortical integration of bilateral nociceptive signals: when more is less. Pain 160(3):724–733.
    1. Page I, Biner E, Descarreaux M (2018) Vertebral displacements and muscle activity during manual therapy: distinct behaviors between spinal manipulation and mobilization. J Manipulative Physiol Ther 41(9):753–761.
    1. Penza CW, Horn ME, George SZ, Bishop MD (2017) Comparison of 2 lumbar manual therapies on temporal summation of pain in healthy volunteers. J Pain 18(11):1397–1408.
    1. Perchet C, Godinho F, Mazza S, Frot M, Legrain V, Magnin M, Garcia-Larrea L (2008) Evoked potentials to nociceptive stimuli delivered by CO2 or Nd:YAP lasers. Clin Neurophysiol 119(11):2615–2622.
    1. Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110(11):1842–1857.
    1. Pickar JG (2002) Neurophysiological effects of spinal manipulation. Spine J 2(5):357–371.
    1. Pickar JG, Bolton PS (2012) Spinal manipulative therapy and somatosensory activation. J Electromyogr Kinesiol 22(5):785–794.
    1. Plaghki L, Mouraux A (2003) How do we selectively activate skin nociceptors with a high power infrared laser? Physiology and biophysics of laser stimulation. Neurophysiol Clin 33(6):269–277
    1. Ploner M, Sorg C, Gross J (2017) Brain rhythms of pain. Trends Cogn Sci 21(2):100–110.
    1. Puhl AA, Reinhart CJ, Doan JB, Vernon H (2017) The quality of placebos used in randomized, controlled trials of lumbar and pelvic joint thrust manipulation-a systematic review. Spine J 17(3):445–456.
    1. Qaseem A, Wilt TJ, McLean RM, Forciea MA (2017) Noninvasive treatments for acute, subacute, and chronic low back pain: a clinical practice guideline from the American College of Physicians. Ann Intern Med 166(7):514–530.
    1. Qiu Y, Inui K, Wang X, Tran TD, Kakigi R (2001) Conduction velocity of the spinothalamic tract in humans as assessed by CO2 laser stimulation of C-fibers. Neurosci Lett 311(3):181–184.
    1. Randoll C, Gagnon-Normandin V, Tessier J, Bois S, Rustamov N, O’Shaughnessy J, Descarreaux M, Piché M (2017) The mechanism of back pain relief by spinal manipulation relies on decreased temporal summation of pain. Neuroscience 349:220–228.
    1. Ronga I, Valentini E, Mouraux A, Iannetti GD (2013) Novelty is not enough: laser-evoked potentials are determined by stimulus saliency, not absolute novelty. J Neurophysiol 109(3):692–701.
    1. Stochkendahl MJ, Kjaer P, Hartvigsen J, Kongsted A, Aaboe J, Andersen M, Andersen MØ, Fournier G, Højgaard B, Jensen MB, Jensen LD (2018) National Clinical Guidelines for non-surgical treatment of patients with recent onset low back pain or lumbar radiculopathy. Eur Spine J 27(1):60–75.
    1. Traeger AC, Buchbinder R, Elshaug AG, Croft PR, Maher CG (2019) Care for low back pain: can health systems deliver? Bull World Health Organ 97(6):423–433.
    1. Triano JJ, Giuliano D, Kanga I, Starmer D, Brazeau J, Screaton CE, Semple C (2015) Consistency and malleability of manipulation performance in experienced clinicians: a pre-post experimental design. J Manipulative Physiol Ther 38(6):407–415.
    1. Wirth B, Gassner A, de Bruin ED, Axen I, Swanenburg J, Humphreys BK, Schweinhardt P (2019) Neurophysiological effects of high velocity and low amplitude spinal manipulation in symptomatic and asymptomatic humans: a systematic literature review. Spine 44(15):E914–E926.

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