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Acta Neurochirurgica

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01-12-2018 | Original Article - Functional Neurosurgery - Pain

Spinal cord stimulation modulates descending pain inhibition and temporal summation of pricking pain in patients with neuropathic pain

Authors: Sigrid Schuh-Hofer, Janina Fischer, Andreas Unterberg, Rolf-Detlef Treede, Rezvan Ahmadi

Published in: Acta Neurochirurgica | Issue 12/2018

Abstract

Background

Spinal cord stimulation (SCS) is an established treatment option for patients with refractory chronic pain conditions. While effects of SCS on dorsal horn neuronal circuitries are intensively studied, current knowledge on the impact of SCS on descending pain pathways is scarce and relies on preclinical data. We aimed to address this topic and hypothesized a significant effect of SCS on descending pain modulation. In light of current efforts to determine the sensitivity of “static” versus “dynamic” somatosensory parameters to characterize pathophysiological pain conditions, all SCS patients were carefully investigated using both classes of somatosensory outcome parameters.

Methods

Descending pain pathways were investigated by using a “Cold Pressor Test.” This test enables to evaluate the efficacy of conditioned pain modulation (CPM) at the individual level. CPM efficacy was assessed in eight neuropathic pain patients (age 55.5 ± 10.6) during the two conditions stimulator “ON” and “OFF.” The impact of SCS on “static” and “dynamic” somatosensory parameters was explored by using a quantitative sensory testing (QST) battery.

Results

CPM efficacy on pressure pain sensitivity was nearly absent during “OFF” (− 1.2 ± 5.6% facilitation), but increased significantly to 16.3 ± 3.4% inhibition during “ON” (p = 0.03). While most “static” nociceptive QST parameters, represented by mechanical/thermal pain thresholds, exhibited only small effects of SCS (p > 0.05), the wind-up ratio was strongly reduced to within the normal range during “ON” (p = 0.04; Cohen’s d = 1.0). Dynamic mechanical allodynia was abolished in six of seven patients.

Conclusions

Our study provides first human evidence for an impact of SCS on descending pain pathways in the dorsolateral funiculus and emphasizes the significance of “dynamic” pain measures like “CPM”-efficacy and “temporal summation” to evaluate SCS treatment effects. Future prospective studies may use these measures of nociceptive processing to predict SCS therapy response.

Ahmed SU, Zhang Y, Chen L, St Hillary K, Cohen A, Vo T, Houghton M, Mao J (2015) Effects of spinal cord stimulation on pain thresholds and sensory perceptions in chronic pain patients. Neuromodulation 18:355–360. https://doi.org/10.1111/ner.12316 CrossRefPubMed

Broggi G, Franzini A, Parati E, Parenty M, Flauto C, Servello D (1985) Neurochemical and structural modifications related to pain control induced by spinal cord stimulation. In: Neurostimulation: An Overview. Futura Publishing, New York, pp 87–95

Cameron T (2004) Safety and efficacy of spinal cord stimulation for the treatment of chronic pain: a 20-year literature review. J Neurosurg 100:254–267PubMed

Campbell C, Bond K, Wacnik P, Williams K, Erdek M, Christo P, Cohen S, Raja S (2012) Alterations in clinical pain and temporal summation following spinal cord stimulation. J Pain 13:S69. https://doi.org/10.1016/j.jpain.2012.01.286 CrossRef

Campbell JN, Taub A (1973) Local analgesia from percutaneous electrical stimulation. A peripheral mechanism. Arch Neurol 28:347–350CrossRef

Chen AC, Treede RD, Bromm B (1985) Tonic pain inhibits phasic pain: evoked cerebral potential correlates in man. Psychiatry Res 14:343–351CrossRef

Chivukula S, Tempel ZJ, Weiner GM, Gande AV, Chen C-J, Ding D, Moossy JJ (2014) Cervical and cervicomedullary spinal cord stimulation for chronic pain: efficacy and outcomes. Clin Neurol Neurosurg 127:33–41. https://doi.org/10.1016/j.clineuro.2014.09.023 CrossRefPubMed

Cui J-G, O'Connor WT, Ungerstedt U, Linderoth B, Meyerson BA (1997) Spinal cord stimulation attenuates augmented dorsal horn release of excitatory amino acids in mononeuropathy via a GABAergic mechanism. Pain 73:87–95. https://doi.org/10.1016/S0304-3959(97)00077-8 CrossRefPubMed

Cui JG, Linderoth B, Meyerson BA (1996) Effects of spinal cord stimulation on touch-evoked allodynia involve GABAergic mechanisms. An experimental study in the mononeuropathic rat. Pain 66:287–295CrossRef

10.

Dong D-s YX, Wan C-f, Liu Y, Zhao L, Xi Q, Cui W, Wang Q, Song T (2017) Efficacy of short-term spinal cord stimulation in acute/subacute zoster-related pain: a retrospective study. Pain physician 20:E633–E645PubMed

11.

Dworkin RH, O’Connor AB, Kent J, Mackey SC, Raja SN, Stacey BR, Levy RM, Backonja M, Baron R, Harke H, Loeser JD, Treede R-D, Turk DC, Wells CD (2013) Interventional management of neuropathic pain: NeuPSIG recommendations. Pain 154:2249–2261. https://doi.org/10.1016/j.pain.2013.06.004 CrossRefPubMedPubMedCentral

12.

Eisenberg E, Backonja MM, Fillingim RB, Pud D, Hord DE, King GW, Stojanovic MP (2006) Quantitative sensory testing for spinal cord stimulation in patients with chronic neuropathic pain. Pain Pract 6:161–165. https://doi.org/10.1111/j.1533-2500.2006.00080.x CrossRefPubMed

13.

Eisenberg E, Burstein Y, Suzan E, Treister R, Aviram J (2015) Spinal cord stimulation attenuates temporal summation in patients with neuropathic pain. Pain 156:381–385. https://doi.org/10.1097/01.j.pain.0000460342.69718.a2 CrossRefPubMed

14.

Eisenberg E, Midbari A, Haddad M, Pud D (2010) Predicting the analgesic effect to oxycodone by 'static' and 'dynamic' quantitative sensory testing in healthy subjects. Pain 151:104–109. https://doi.org/10.1016/j.pain.2010.06.025 CrossRefPubMed

15.

Gierthmuhlen J, Maier C, Baron R, Tolle T, Treede RD, Birbaumer N, Huge V, Koroschetz J, Krumova EK, Lauchart M, Maihofner C, Richter H, Westermann A (2012) Sensory signs in complex regional pain syndrome and peripheral nerve injury. Pain 153:765–774. https://doi.org/10.1016/j.pain.2011.11.009 CrossRefPubMed

16.

Grabow TS, Tella PK, Raja SN (2003) Spinal cord stimulation for complex regional pain syndrome: an evidence-based medicine review of the literature. Clin J Pain 19:371–383CrossRef

17.

Gröne E, Crispin A, Fleckenstein J, Irnich D, Treede R-D, Lang PM (2012) Test order of quantitative sensory testing facilitates mechanical hyperalgesia in healthy volunteers. J Pain 13:73–80. https://doi.org/10.1016/j.jpain.2011.10.005 CrossRefPubMed

18.

Guan Y (2012) Spinal cord stimulation: neurophysiological and neurochemical mechanisms of action. Curr Pain Headache Rep 16:217–225. https://doi.org/10.1007/s11916-012-0260-4 CrossRefPubMed

19.

Guan Y, Wacnik PW, Yang F, Carteret AF, Chung CY, Meyer RA, Raja SN (2010) Spinal cord stimulation-induced analgesia: electrical stimulation of dorsal column and dorsal roots attenuates dorsal horn neuronal excitability in neuropathic rats. Anesthesiology 113:1392–1405. https://doi.org/10.1097/ALN.0b013e3181fcd95c CrossRefPubMed

20.

Kapural L, Peterson E, Provenzano DA, Staats P (2017) Clinical evidence for spinal cord stimulation for failed back surgery syndrome (FBSS): systematic review. Spine (Phila Pa 1976) 42(Suppl 14):S61–S66. https://doi.org/10.1097/BRS.0000000000002213 CrossRef

21.

Kemler MA, Reulen JP, Barendse GA, van Kleef M, de Vet HC, van den Wildenberg FA (2001) Impact of spinal cord stimulation on sensory characteristics in complex regional pain syndrome type I: a randomized trial. Anesthesiology 95:72–80CrossRef

22.

Kumar K, Taylor RS, Jacques L, Eldabe S, Meglio M, Molet J, Thomson S, O'Callaghan J, Eisenberg E, Milbouw G, Buchser E, Fortini G, Richardson J, North RB (2008) 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 63:762–770. https://doi.org/10.1227/01.NEU.0000325731.46702.D9 CrossRefPubMed

23.

Levin BE, Hubschmann OR (1980) Dorsal column stimulation. Effect on human cerebrospinal fluid and plasma catecholamines 30:65–71. https://doi.org/10.1212/wnl.30.1.65 CrossRef

24.

Lindblom U, Meyerson BA (1975) Influence on touch, vibration and cutaneous pain of dorsal column stimulation in man. PAIN 1:257–270. https://doi.org/10.1016/0304-3959(75)90042-1 CrossRefPubMed

25.

Linderoth B, Gazelius B, Franck J, Brodin E (1992) Dorsal column stimulation induces release of serotonin and substance P in the cat dorsal horn. Neurosurgery 31:289–297. https://doi.org/10.1227/00006123-199208000-00014 CrossRefPubMed

26.

Mackey IG, Dixon EA, Johnson K, Kong JT (2017) Dynamic quantitative sensory testing to characterize central pain processing. J Vis Exp. https://doi.org/10.3791/54452

27.

Maier C, Baron R, Tölle TR, Binder A, Birbaumer N, Birklein F, Gierthmühlen J, Flor H, Geber C, Huge V, Krumova EK, Landwehrmeyer GB, Magerl W, Maihöfner C, Richter H, Rolke R, Scherens A, Schwarz A, Sommer C, Tronnier V, Üçeyler N, Valet M, Wasner G, Treede RD (2010) Quantitative sensory testing in the German research network on neuropathic pain (DFNS): somatosensory abnormalities in 1236 patients with different neuropathic pain syndromes. Pain 150:439–450. https://doi.org/10.1016/j.pain.2010.05.002 CrossRefPubMed

28.

Marchand S, Bushnell MC, Molina-Negro P, Martinez SN, Duncan GH (1991) The effects of dorsal column stimulation on measures of clinical and experimental pain in man. Pain 45:249–257CrossRef

29.

Marcuzzi A, Wrigley PJ, Dean CM, Adams R, Hush JM (2017) The long-term reliability of static and dynamic quantitative sensory testing in healthy individuals. Pain 158:1217–1223. https://doi.org/10.1097/j.pain.0000000000000901 CrossRefPubMed

30.

Meier K, Nikolajsen L, Sorensen JC, Jensen TS (2015) Effect of spinal cord stimulation on sensory characteristics: a randomized, blinded crossover study. Clin J Pain 31:384–392. https://doi.org/10.1097/ajp.0000000000000131 CrossRefPubMed

31.

Melzack R, Wall PD (1965) Pain mechanisms: a new theory. Science 150:971–979CrossRef

32.

Nir RR, Yarnitsky D (2015) Conditioned pain modulation. Curr Opin Support Palliat care 9:131–137. https://doi.org/10.1097/spc.0000000000000126 CrossRefPubMed

33.

Piva B, Shaladi A, Saltari R, Gilli G (2003) Spinal cord stimulation in the management of pain from brachial plexus avulsion. Neuromodulation: Technology at the Neural Interface 6:27–31. https://doi.org/10.1046/j.1525-1403.2003.03004.x CrossRef

34.

Rasche D, Ruppolt MA, Kress B, Unterberg A, Tronnier VM (2006) Quantitative sensory testing in patients with chronic unilateral radicular neuropathic pain and active spinal cord stimulation. Neuromodulation 9:239–247. https://doi.org/10.1111/j.1525-1403.2006.00066.x CrossRefPubMed

35.

Reitz MC, Hrncic D, Treede RD, Caspani O (2016) A comparative behavioural study of mechanical hypersensitivity in 2 pain models in rats and humans. Pain 157:1248–1258. https://doi.org/10.1097/j.pain.0000000000000515 CrossRefPubMed

36.

Rolke R, Baron R, Maier C, Tolle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Botefur IC, Braune S, Flor H, Huge V, Klug R, Landwehrmeyer GB, Magerl W, Maihofner C, Rolko C, Schaub C, Scherens A, Sprenger T, Valet M, Wasserka B (2006) Quantitative sensory testing in the German research network on neuropathic pain (DFNS): standardized protocol and reference values. Pain 123:231–243. https://doi.org/10.1016/j.pain.2006.01.041 CrossRefPubMed

37.

Saadé NE, Barchini J, Tchachaghian S, Chamaa F, Jabbur SJ, Song Z, Meyerson BA, Linderoth B (2015) The role of the dorsolateral funiculi in the pain relieving effect of spinal cord stimulation: a study in a rat model of neuropathic pain. Exp Brain Res 233:1041–1052. https://doi.org/10.1007/s00221-014-4180-x CrossRefPubMed

38.

Saade NE, Tabet MS, Atweh SF, Jabbur SJ (1984) Modulation of segmental mechanisms by activation of a dorsal column brainstem spinal loop. Brain Res 310:180–184CrossRef

39.

Shealy CN, Mortimer JT, Reswick JB (1967) Electrical inhibition of pain by stimulation of the dorsal columns: preliminary clinical report. Anesth Analg 46:489–491PubMed

40.

Smits H, Ultenius C, Deumens R, Koopmans GC, Honig WM, van Kleef M, Linderoth B, Joosten EA (2006) Effect of spinal cord stimulation in an animal model of neuropathic pain relates to degree of tactile "allodynia". Neuroscience 143:541–546. https://doi.org/10.1016/j.neuroscience.2006.08.007 CrossRefPubMed

41.

Song Z, Ansah OB, Meyerson BA, Pertovaara A, Linderoth B (2013) The rostroventromedial medulla is engaged in the effects of spinal cord stimulation in a rodent model of neuropathic pain. Neuroscience 247:134–144. https://doi.org/10.1016/j.neuroscience.2013.05.027 CrossRefPubMed

42.

Taylor RS Spinal cord stimulation in complex regional pain syndrome and refractory neuropathic back and leg pain/failed back surgery syndrome: results of a systematic review and meta-analysis. J Pain Symptom Manag 31:S13–S19. https://doi.org/10.1016/j.jpainsymman.2005.12.010 CrossRef

43.

Tazawa T, Kamiya Y, Kobayashi A, Saeki K, Takiguchi M, Nakahashi Y, Shinbori H, Funakoshi K, Goto T (2015) Spinal cord stimulation modulates supraspinal centers of the descending antinociceptive system in rats with unilateral spinal nerve injury. Mol Pain 11:36. https://doi.org/10.1186/s12990-015-0039-9 CrossRefPubMedPubMedCentral

44.

van Eijs F, Geurts JW, Van Zundert J, Faber CG, Kessels AG, Joosten EA, van Kleef M (2012) Spinal cord stimulation in complex regional pain syndrome type I of less than 12-month duration. Neuromodulation: Technology at the Neural Interface 15:144–150. https://doi.org/10.1111/j.1525-1403.2011.00424.x CrossRef

45.

van Eijs F, Smits H, Geurts JW, Kessels AG, Kemler MA, van Kleef M, Joosten EA, Faber CG (2010) Brush-evoked allodynia predicts outcome of spinal cord stimulation in complex regional pain syndrome type 1. Eur J Pain 14:164–169. https://doi.org/10.1016/j.ejpain.2009.10.009 CrossRefPubMed

46.

Villanueva L, Peschanski M, Calvino B, Le Bars D (1986) Ascending pathways in the spinal cord involved in triggering of diffuse noxious inhibitory controls in the rat. J Neurophysiol 55:34–55. https://doi.org/10.1152/jn.1986.55.1.34 CrossRefPubMed

47.

Visnjevac O, Costandi S, Patel BA, Azer G, Agarwal P, Bolash R, Mekhail NA (2017) A comprehensive outcome-specific review of the use of spinal cord stimulation for complex regional pain syndrome. Pain Practice 17:533–545. https://doi.org/10.1111/papr.12513 CrossRefPubMed

48.

Wall PD, Sweet WH (1967) Temporary abolition of pain in man. Science 155:108–109CrossRef

49.

Williams KA, Gonzalez-Fernandez M, Hamzehzadeh S, Wilkinson I, Erdek MA, Plunkett A, Griffith S, Crooks M, Larkin T, Cohen SP (2011) A multi-center analysis evaluating factors associated with spinal cord stimulation outcome in chronic pain patients. Pain Med 12:1142–1153. https://doi.org/10.1111/j.1526-4637.2011.01184.x CrossRefPubMed

50.

Yakhnitsa V, Linderoth B, Meyerson BA (1999) Spinal cord stimulation attenuates dorsal horn neuronal hyperexcitability in a rat model of mononeuropathy. Pain 79:223–233CrossRef

51.

Yarnitsky D (2010) Conditioned pain modulation (the diffuse noxious inhibitory control-like effect): its relevance for acute and chronic pain states. Curr Opin Anaesthesiol 23:611–615. https://doi.org/10.1097/ACO.0b013e32833c348b CrossRefPubMed

52.

Yarnitsky D, Bouhassira D, Drewes AM, Fillingim RB, Granot M, Hansson P, Landau R, Marchand S, Matre D, Nilsen KB, Stubhaug A, Treede RD, Wilder-Smith OHG (2015) Recommendations on practice of conditioned pain modulation (CPM) testing. Eur J Pain 19:805–806. https://doi.org/10.1002/ejp.605 CrossRefPubMed

53.

Yarnitsky D, Granot M, Nahman-Averbuch H, Khamaisi M, Granovsky Y (2012) Conditioned pain modulation predicts duloxetine efficacy in painful diabetic neuropathy. Pain 153:1193–1198. https://doi.org/10.1016/j.pain.2012.02.021 CrossRefPubMed

Title: Spinal cord stimulation modulates descending pain inhibition and temporal summation of pricking pain in patients with neuropathic pain
Authors: Sigrid Schuh-Hofer
Janina Fischer
Andreas Unterberg
Rolf-Detlef Treede
Rezvan Ahmadi
Publication date: 01-12-2018
Publisher: Springer Vienna
Published in: Acta Neurochirurgica / Issue 12/2018
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-018-3669-7

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Spinal cord stimulation modulates descending pain inhibition and temporal summation of pricking pain in patients with neuropathic pain

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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