Advertisement

Observing Altered Nociceptive Detection Thresholds in Patients With Persistent Spinal Pain Syndrome Type 2 With a Dorsal Root Ganglion Stimulator

  • Tom Berfelo
    Correspondence
    Address correspondence to: Tom Berfelo, MSc, Department of Anesthesiology, Intensive Care and Pain Medicine, St. Antonius Hospital, PO Box 2500, 3430 EM, Nieuwegein, The Netherlands.
    Affiliations
    Department of Anesthesiology, Intensive Care and Pain Medicine, St. Antonius Hospital, Nieuwegein, The Netherlands

    Department of Biomedical Signals and Systems, Technical Medical (TechMed) Centre, University of Twente, Enschede, The Netherlands
    Search for articles by this author
  • Robert-Jan Doll
    Affiliations
    Department of Biomedical Signals and Systems, Technical Medical (TechMed) Centre, University of Twente, Enschede, The Netherlands

    Centre for Human Drug Research, Leiden, The Netherlands
    Search for articles by this author
  • Imre Poldino Krabbenbos
    Affiliations
    Department of Anesthesiology, Intensive Care and Pain Medicine, St. Antonius Hospital, Nieuwegein, The Netherlands
    Search for articles by this author
  • Jan Reinoud Buitenweg
    Affiliations
    Department of Biomedical Signals and Systems, Technical Medical (TechMed) Centre, University of Twente, Enschede, The Netherlands
    Search for articles by this author
Published:December 18, 2021DOI:https://doi.org/10.1016/j.neurom.2021.10.023

      Abstract

      Objectives

      There is a lack of clinically relevant measures for quantification of maladaptive mechanisms of the nociceptive system leading to chronic pain. Recently, we developed a method that tracks nociceptive detection thresholds (NDTs) using intraepidermal electrical stimulation. In this study, we explored the feasibility of using this NDT method in patients with persistent spinal pain syndrome type 2 (PSPS-T2) and its potential to enable observation of altered nociceptive processing induced by dorsal root ganglion (DRG) stimulation. In addition, we compared NDTs with quantitative sensory testing (QST) measurements and numeric rating scale (NRS).

      Materials and Methods

      A total of 12 patients with PSPS-T2 (seven men; 60.4 ± 12.3 years) experiencing chronic unilateral lower limb pain treated with DRG stimulation were included in the study. Both the NDT method and electrical and pressure QST methods were performed twice in the L5 dermatome on both the affected and the unaffected foot, once with the DRG stimulator turned off and, subsequently, once with the DRG stimulator turned on.

      Results

      The NDT method can be applied to patients with PSPS-T2. With the DRG stimulator turned off, NDTs on the affected side were significantly higher than on the unaffected side. This difference was no longer present once the DRG stimulator was turned on. Furthermore, DRG stimulation affected QST (electrical and pressure) values and NRS scores. Finally, NDTs showed larger contrasts between the sides than QST measures.

      Conclusions

      The NDT method permitted observation of altered nociceptive function. The effect of DRG stimulation also was reflected in QST outcomes and NRS scores. The larger contrast between the sides for NDTs suggests that the NDT method might be valuable for future quantification of nociceptive dysfunction in chronic pain.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Cohen S.P.
        • Vase L.
        • Hooten W.M.
        Chronic pain: an update on burden, best practices, and new advances.
        Lancet. 2021; 397: 2082-2097https://doi.org/10.1016/S0140-6736(21)00393-7
        • Attal N.
        • Perrot S.
        • Fermanian J.
        • Bouhassira D.
        The neuropathic components of chronic low back pain: a prospective multicenter study using the DN4 questionnaire.
        J Pain. 2011; 12: 1080-1087https://doi.org/10.1016/j.jpain.2011.05.006
        • Main C.J.
        Pain assessment in context: a state of the science review of the McGill pain questionnaire 40 years on.
        Pain. 2016; 157: 1387-1399https://doi.org/10.1097/j.pain.0000000000000457
        • Ylinen J.
        • Nykänen M.
        • Kautiainen H.
        • Häkkinen A.
        Evaluation of repeatability of pressure algometry on the neck muscles for clinical use.
        Man Ther. 2007; 12: 192-197https://doi.org/10.1016/j.math.2006.06.010
        • Pelfort X.
        • Torres-Claramunt R.
        • Sánchez-Soler J.F.
        • et al.
        Pressure algometry is a useful tool to quantify pain in the medial part of the knee: an intra- and inter-reliability study in healthy subjects.
        Orthop Traumatol Surg Res. 2015; 101: 559-563https://doi.org/10.1016/j.otsr.2015.03.016
        • Stuginski-Barbosa J.
        • Silva R.S.
        • Cunha C.O.
        • Bonjardim L.R.
        • Conti A.C.C.F.
        • Conti P.C.R.
        Pressure pain threshold and pain perception in temporomandibular disorder patients: is there any correlation?.
        Rev Dor. 2015; 16: 22-26https://doi.org/10.5935/1806-0013.20150005
        • Park G.
        • Kim C.W.
        • Park S.B.
        • Kim M.J.
        • Jang S.H.
        Reliability and usefulness of the pressure pain threshold measurement in patients with myofascial pain.
        Ann Rehabil Med. 2011; 35: 412-417https://doi.org/10.5535/arm.2011.35.3.412
        • Inceu G.V.
        • Veresiu I.A.
        Measurement of current perception thresholds using the Neurometer® — applicability in diabetic neuropathy.
        Clujul Med. 2015; 88: 449-452https://doi.org/10.15386/cjmed-491
        • Imoto K.
        • Takebayashi T.
        • Kanaya K.
        • Kawaguchi S.
        • Katahira G.
        • Yamashita T.
        Quantitative analysis of sensory functions after lumbar discectomy using current perception threshold testing.
        Eur Spine J. 2007; 16: 971-975https://doi.org/10.1007/s00586-006-0285-7
        • Savic G.
        • Bergström E.M.K.
        • Frankel H.L.
        • Jamous M.A.
        • Ellaway P.H.
        • Davey N.J.
        Perceptual threshold to cutaneous electrical stimulation in patients with spinal cord injury.
        Spinal Cord. 2006; 44: 560-566https://doi.org/10.1038/sj.sc.3101921
        • Yamashita T.
        • Kanaya K.
        • Sekine M.
        • Takebayashi T.
        • Kawaguchi S.
        • Katahira G.
        A quantitative analysis of sensory function in lumbar radiculopathy using current perception threshold testing.
        Spine (Phila Pa 1976). 2002; 27: 1567-1570https://doi.org/10.1097/00007632-200207150-00016
        • Hansson P.
        • Backonja M.
        • Bouhassira D.
        Usefulness and limitations of quantitative sensory testing: clinical and research application in neuropathic pain states.
        Pain. 2007; 129: 256-259https://doi.org/10.1016/j.pain.2007.03.030
        • Birklein F.
        • Sommer C.
        Pain: quantitative sensory testing—a tool for daily practice?.
        Nat Rev Neurol. 2013; 9: 490-492https://doi.org/10.1038/nrneurol.2013.157
        • Backonja M.M.
        • Attal N.
        • Baron R.
        • et al.
        Value of quantitative sensory testing in neurological and pain disorders: NeuPSIG consensus.
        Pain. 2013; 154: 1807-1819https://doi.org/10.1016/j.pain.2013.05.047
        • Van der Cruyssen F.
        • Van Tieghem L.
        • Croonenborghs T.M.
        • et al.
        Orofacial quantitative sensory testing: current evidence and future perspectives.
        Eur J Pain. 2020; 24: 1425-1439https://doi.org/10.1002/ejp.1611
        • Doll R.J.
        • Buitenweg J.R.
        • Meijer H.G.E.
        • Veltink P.H.
        Tracking of nociceptive thresholds using adaptive psychophysical methods.
        Behav Res Methods. 2014; 46: 55-66https://doi.org/10.3758/s13428-013-0368-4
        • Inui K.
        • Tran T.D.
        • Hoshiyama M.
        • Kakigi R.
        Preferential stimulation of Aδ fibers by intra-epidermal needle electrode in humans.
        Pain. 2002; 96: 247-252
        • Inui K.
        • Kakigi R.
        Pain perception in humans: use of intraepidermal electrical stimulation.
        J Neurol Neurosurg Psychiatry. 2012; 83: 551-556https://doi.org/10.1136/jnnp-2011-301484
        • Mouraux A.
        • Iannetti G.D.
        • Plaghki L.
        Low intensity intra-epidermal electrical stimulation can activate Adelta-nociceptors selectively.
        Pain. 2010; 150: 199-207https://doi.org/10.1016/j.pain.2010.04.026
        • Doll R.J.
        • Maten A.C.A.
        • Spaan S.P.G.
        • Veltink P.H.
        • Buitenweg J.R.
        Effect of temporal stimulus properties on the nociceptive detection probability using intra-epidermal electrical stimulation.
        Exp Brain Res. 2016; 234: 219-227https://doi.org/10.1007/s00221-015-4451-1
        • Liang M.
        • Lee M.C.
        • O’Neill J.
        • Dickenson A.H.
        • Iannetti G.D.
        Brain potentials evoked by intraepidermal electrical stimuli reflect the central sensitization of nociceptive pathways.
        J Neurophysiol. 2016; 116: 286-295https://doi.org/10.1152/jn.00013.2016
        • Harte S.E.
        • Harris R.E.
        • Clauw D.J.
        The neurobiology of central sensitization.
        J Appl Biobehav Res. 2018; 23https://doi.org/10.1111/jabr.12137
        • Van den Berg B.
        • Buitenweg J.R.
        Observation of nociceptive processing: effect of intra-epidermal electric stimulus properties on detection probability and evoked potentials.
        Brain Topogr. 2021; 34: 139-153https://doi.org/10.1007/s10548-020-00816-y
        • Doll R.J.
        • van Amerongen G.
        • Hay J.L.
        • Groeneveld G.J.
        • Veltink P.H.
        • Buitenweg J.R.
        Responsiveness of electrical nociceptive detection thresholds to capsaicin (8%)-induced changes in nociceptive processing.
        Exp Brain Res. 2016; 234: 2505-2514
        • Doll R.J.
        • Veltink P.H.
        • Buitenweg J.R.
        Observation of time-dependent psychophysical functions and accounting for threshold drifts.
        Atten Percept Psychophys. 2015; 77: 1440-1447https://doi.org/10.3758/s13414-015-0865-x
        • van den Berg B.
        • Doll R.J.
        • Mentink A.L.H.
        • Siebenga P.S.
        • Groeneveld G.J.
        • Buitenweg J.R.
        Simultaneous tracking of psychophysical detection thresholds and evoked potentials to study nociceptive processing.
        Behav Res Methods. 2020; 52: 1617-1628https://doi.org/10.3758/s13428-019-01338-7
        • Blond S.
        • Mertens P.
        • David R.
        • Roulaud M.
        • Rigoard P.
        From “mechanical” to “neuropathic” back pain concept in FBSS patients. A systematic review based on factors leading to the chronification of pain (part C).
        Neurochirurgie. 2015; 61: S45-S56
        • Groen G.J.
        • Beese U.H.
        • Van de Kelft E.
        • Groen R.J.M.
        A practical approach to the diagnosis and understanding of chronic low back pain, based on its pathophysiology.
        in: van de Kelft E. Surgery of the Spine and Spinal Cord: A Neurosurgical Approach. Springer, 2016: 359-381https://doi.org/10.1007/978-3-319-27613-7_22
        • Van Buyten J.P.
        Neurostimulation for the management of failed back surgery syndrome (FBSS).
        in: van de Kelft E. Surgery of the Spine and Spinal Cord: A Neurosurgical Approach. Springer, 2016: 585-600https://doi.org/10.1007/978-3-319-27613-7_37
        • Fitzcharles M.A.
        • Cohen S.P.
        • Clauw D.J.
        • Littlejohn G.
        • Usui C.
        • Häuser W.
        Nociplastic pain: towards an understanding of prevalent pain conditions.
        Lancet. 2021; 397: 2098-2110https://doi.org/10.1016/S0140-6736(21)00392-5
        • Liem L.
        Stimulation of the dorsal root ganglion.
        Prog Neurol Surg. 2015; 29: 213-224https://doi.org/10.1159/000434673
        • Poláček H.
        • Kozák J.
        • Vrba I.
        • Vrána J.
        • Stančák A.
        Effects of spinal cord stimulation on the cortical somatosensory evoked potentials in failed back surgery syndrome patients.
        Clin Neurophysiol. 2007; 118: 1291-1302https://doi.org/10.1016/j.clinph.2007.02.029
        • De Andrade D.C.
        • Bendib B.
        • Hattou M.
        • Keravel Y.
        • Nguyen J.P.
        • Lefaucheur J.P.
        Neurophysiological assessment of spinal cord stimulation in failed back surgery syndrome.
        Pain. 2010; 150: 485-491https://doi.org/10.1016/j.pain.2010.06.001
        • Van Buyten J.P.
        Neurostimulation for chronic neuropathic back pain in failed back surgery syndrome.
        J Pain Symptom Manage. 2006; 31 (S25–S29)
        • Knotkova H.
        • Hamani C.
        • Sivanesan E.
        • et al.
        Neuromodulation for chronic pain.
        Lancet. 2021; 397: 2111-2124https://doi.org/10.1016/S0140-6736(21)00794-7
        • Liem L.
        • Russo M.
        • Huygen F.J.P.M.
        • et al.
        One-year outcomes of spinal cord stimulation of the dorsal root ganglion in the treatment of chronic neuropathic pain.
        Neuromodulation. 2015; 18: 41-48
        • Huygen F.J.P.M.
        • Liem L.
        • Nijhuis H.
        • Cusack W.
        • Kramer J.
        Evaluating dorsal root ganglion stimulation in a prospective Dutch cohort.
        Neuromodulation. 2019; 22: 80-86https://doi.org/10.1111/ner.12798
        • Bates D.
        • Mächler M.
        • Bolker B.M.
        • Walker S.C.
        Fitting linear mixed-effects models using lme4.
        J Stat Softw. 2015; 67https://doi.org/10.18637/jss.v067.i01
      1. R Core Team. R: a language and environment for statistical computing. Vienna, Austria. 2018. Accessed December 6, 2021. https://www.R-project.org/

        • Faraggi D.
        • Izikson P.
        • Reiser B.
        Confidence intervals for the 50 per cent response dose.
        Stat Med. 2003; 22: 1977-1988https://doi.org/10.1002/sim.1368
        • Moscatelli A.
        • Mezzetti M.
        • Lacquaniti F.
        Modeling psychophysical data at the population-level: the generalized linear mixed model.
        J Vis. 2012; 12: 1-17https://doi.org/10.1167/12.11.26
        • Ramaswamy S.
        • Wodehouse T.
        • Langford R.
        • Thomson S.
        • Taylor R.
        • Mehta V.
        Characterizing the somatosensory profile of patients with failed back surgery syndrome with unilateral lumbar radiculopathy undergoing spinal cord stimulation: a single center prospective pilot study.
        Neuromodulation. 2019; 22: 333-340https://doi.org/10.1111/ner.12862
        • Taylor R.S.
        • Desai M.J.
        • Rigoard P.
        • Taylor R.J.
        Predictors of pain relief following spinal cord stimulation in chronic back and leg pain and failed back surgery syndrome: a systematic review and meta-regression analysis.
        Pain Pract. 2014; 14: 489-505https://doi.org/10.1111/papr.12095
        • Kumar K.
        • Taylor R.S.
        • Jacques L.
        • et al.
        The effects of spinal cord stimulation in neuropathic pain are sustained: a 24-month follow-up of the prospective randomized controlled multicenter trial of the effectiveness of spinal cord stimulation.
        Neurosurgery. 2008; 63: 762-770
        • Rigoard P.
        • Gatzinsky K.
        • Deneuville J.P.
        • et al.
        Optimizing the management and outcomes of failed back surgery syndrome: a consensus statement on definition and outlines for patient assessment.
        Pain Res Manag. 2019; 2019: 3126464https://doi.org/10.1155/2019/3126464
        • Goudman L.
        • Huysmans E.
        • Coppieters I.
        • et al.
        Electrical (pain) thresholds and conditioned pain modulation in patients with low back-related leg pain and patients with failed back surgery syndrome: a cross-sectional pilot study.
        Pain Med. 2020; 21: 538-547https://doi.org/10.1093/pm/pnz118
        • Chesterton L.S.
        • Sim J.
        • Wright C.C.
        • Foster N.E.
        Interrater reliability of algometry in measuring pressure pain thresholds in healthy humans, using multiple raters.
        Clin J Pain. 2007; 23: 760-766https://doi.org/10.1097/AJP.0b013e318154b6ae
        • Koetsier E.
        • Franken G.
        • Debets J.
        • et al.
        Dorsal root ganglion stimulation in experimental painful diabetic polyneuropathy: delayed wash-out of pain relief after low-frequency (1 Hz) stimulation.
        Neuromodulation. 2020; 23: 177-184https://doi.org/10.1111/ner.13048
        • Parker T.
        • Green A.
        • Aziz T.
        Rapid onset and short washout periods of dorsal root ganglion stimulation facilitate multiphase crossover study designs.
        Brain Stimul. 2019; 12: 1617-1618https://doi.org/10.1016/j.brs.2019.08.015
        • Chapman K.B.
        • Yousef T.A.
        • Vissers K.C.
        • van Helmond N.D.
        • Stanton-Hicks M.D.
        Very low frequencies maintain pain relief from dorsal root ganglion stimulation: an evaluation of dorsal root ganglion neurostimulation frequency tapering.
        Neuromodulation. 2021; 24: 746-752https://doi.org/10.1111/ner.13322
        • Chapman K.B.
        • Yousef T.A.
        • Foster A.
        • Stanton-Hicks M.D.
        • van Helmond N.
        Mechanisms for the clinical utility of low-frequency stimulation in neuromodulation of the dorsal root ganglion.
        Neuromodulation. 2021; 24: 738-745https://doi.org/10.1111/ner.13323