Biomarkers for predicting central neuropathic pain occurrence and severity after spinal cord injury: results of a long-term longitudinal study.
Journal
Pain
ISSN: 1872-6623
Titre abrégé: Pain
Pays: United States
ID NLM: 7508686
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
pubmed:
7
11
2019
medline:
9
2
2021
entrez:
7
11
2019
Statut:
ppublish
Résumé
Central neuropathic pain (CNP) after spinal cord injury (SCI) is debilitating and immensely impacts the individual. Central neuropathic pain is relatively resistant to treatment administered after it develops, perhaps owing to irreversible pathological processes. Although preemptive treatment may overcome this shortcoming, its administration necessitates screening patients with clinically relevant biomarkers that could predict CNP early post-SCI. The aim was to search for such biomarkers by measuring pronociceptive and for the first time, antinociceptive indices early post-SCI. Participants were 47 patients with acute SCI and 20 healthy controls. Pain adaptation, conditioned pain modulation (CPM), pain temporal summation, wind-up pain, and allodynia were measured above, at, and below the injury level, at 1.5 months after SCI. Healthy control were tested at corresponding regions. Spinal cord injury patients were monitored for CNP emergence and characteristics at 3 to 4, 6 to 7, and 24 months post-SCI. Central neuropathic pain prevalence was 57.4%. Central neuropathic pain severity, quality, and aggravating factors but not location somewhat changed over 24 months. Spinal cord injury patients who eventually developed CNP exhibited early, reduced at-level pain adaptation and CPM magnitudes than those who did not. The best predictor for CNP emergence at 3 to 4 and 7 to 8 months was at-level pain adaptation with odds ratios of 3.17 and 2.83, respectively (∼77% probability) and a cutoff value with 90% sensitivity. Allodynia and at-level CPM predicted CNP severity at 3 to 4 and 24 months, respectively. Reduced pain inhibition capacity precedes, and may lead to CNP. At-level pain adaptation is an early CNP biomarker with which individuals at risk can be identified to initiate preemptive treatment.
Identifiants
pubmed: 31693542
doi: 10.1097/j.pain.0000000000001740
pii: 00006396-202003000-00011
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
545-556Références
Albu S, Gómez-Soriano J, Avila-Martin G, Taylor J. Deficient conditioned pain modulation after spinal cord injury correlates with clinical spontaneous pain measures. PAIN 2015;156:260–72.
Attal N, Mazaltarine G, Perrouin-Verbe B, Albert T. Chronic neuropathic pain management in spinal cord injury patients. What is the efficacy of pharmacological treatments with a general mode of administration? (oral, transdermal, intravenous). Ann Phys Rehabil Med 2009;52:124–41.
Bingel U, Herken W, Teutsch S, May A. Habituation to painful stimulation involves the antinociceptive system—A 1-year follow-up of 10 participants. PAIN 2008;140:393–4.
Bryce TN, Biering-Sørensen F, Finnerup NB, Cardenas DD, Defrin R, Lundeberg T, Norrbrink C, Richards JS, Siddall P, Stripling T, Treede RD, Waxman SG, Widerström-Noga E, Yezierski RP, Dijkers M. International spinal cord injury pain classification: part I. Background and description. Spinal Cord 2012;50:413–7.
Budh CN, Lund I, Ertzgaard P, Holtz A, Hultling C, Levi R, Werhagen L, Lundeberg T. Pain in a Swedish spinal cord injury population. Clin Rehabil 2003;17:685–90.
Burke D, Fullen BM, Stokes D, Lennon O. Neuropathic pain prevalence following spinal cord injury: a systematic review and meta-analysis. Eur J Pain 2017;21:29–44.
Coghill RC, Mayer DJ, Price DD. Wide dynamic range but not nociceptive-specific neurons encode multidimensional features of prolonged repetitive heat pain. J Neurophysiol 1993;69:703–16.
Coronel MF, Villar MJ, Brumovsky PR, González SL. Spinal neuropeptide expression and neuropathic behavior in the acute and chronic phases after spinal cord injury: effects of progesterone administration. Peptides 2017;88:189–95.
Cruz-Almeida Y, Martinez-Arizala A, Widerström-Noga EG. Chronicity of pain associated with spinal cord injury: a longitudinal analysis. J Rehabil Res Dev 2005;42:585–94.
Cruz-Almeida Y, Felix ER, Martinez-Arizala A, Widerström-Noga EG. Decreased spinothalamic and dorsal column medial lemniscus-mediated function is associated with neuropathic pain after spinal cord injury. J Neurotrauma 2012;29:2706–15.
Defrin R, Ohry A, Blumen N, Urca G. Characterization of chronic pain and somatosensory function in spinal cord injury subjects. PAIN 2001;89:253–63.
Dickenson AH, Sullivan AF. Evidence for a role of the NMDA receptor in the frequency dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation. Neuropharmacology 1987;26:1235–8.
Ducreux D, Attal N, Parker F, Bouhassira D. Mechanisms of central neuropathic pain: a combined psychophysical and fMRI study in syringomyelia. Brain 2006;129:963–76.
Eide PK, Jørum E, Stenehjem AE. Somatosensory findings in patients with spinal cord injury and central dysaesthesia pain. J Neurol Neurosurg Psychiatry 1996;60:411–15.
Finnerup NB, Yezierski RP, Sang CN, Burchiel KJ, Jensen TS. Treatment of spinal cord injury pain. Pain Clin Updates 2001;9:1–6.
Finnerup NB, Johannesen IL, Fuglsang-Frederiksen A, Bach FW, Jensen TS. Sensory function in spinal cord injury patients with and without central pain. Brain 2003;126:57–70.
Finnerup NB, Jensen TS. Clinical use of pregabalin in the management of central neuropathic pain. Neuropsychiatr Dis Treat 2007;3:885–91.
Finnerup NB, Pedersen LH, Terkelsen AJ, Johannesen IL, Jensen TS. Reaction to topical capsaicin in spinal cord injury patients with and without central pain. Exp Neurol 2007;205:190–200.
Finnerup NB, Norrbrink C, Trok K, Piehl F, Johannesen IL, Sørensen JC, Jensen TS, Werhagen L. Phenotypes and predictors of pain following traumatic spinal cord injury: a prospective study. J Pain 2014;15:40–8.
Finnerup NB, Attal N, Haroutounian S, McNicol E, Baron R, Dworkin RH, Gilron I, Haanpää M, Hansson P, Jensen TS, Kamerman PR, Lund K, Moore A, Raja SN, Rice AS, Rowbotham M, Sena E, Siddall P, Smith BH, Wallace M. Pharmacotherapy for neuropathic pain in adults: a systematic review and meta-analysis. Lancet Neurol 2015;14:162–73.
Finnerup NB, Jensen MP, Norrbrink C, Trok K, Johannesen IL, Jensen TS, Werhagen L. A prospective study of pain and psychological functioning following traumatic spinal cord injury. Spinal Cord 2016;54:816–21.
Geva N, Defrin R. Enhanced pain modulation among triathletes: a possible explanation for their exceptional capabilities. PAIN 2013;154:2317–23.
Granot M, Granovsky Y, Sprecher E, Nir RR, Yarnitsky D. Contact heat-evoked temporal summation: tonic versus repetitive-phasic stimulation. PAIN 2006;122:295–305.
Gruener H, Zeilig G, Laufer Y, Blumen N, Defrin R. Differential pain modulation properties in central neuropathic pain after spinal cord injury. PAIN 2016;157:1415–24.
Gwak YS, Crown ED, Unabia GC, Hulsebosch CE. Propentofylline attenuates allodynia, glial activation and modulates GABAergic tone after spinal cord injury in the rat. PAIN 2008;138:410–22.
Hatch MN, Cushing TR, Carlson GD, Chang EY. Neuropathic pain and SCI: identification and treatment strategies in the 21st century. J Neurol Sci 2018;384:75–83.
Heinricher MM, Fields HL. Central nervous system mechanisms of pain modulation. In: Wall and Melzack's textbook of pain. 6th ed. Philadelphia, PA: Saunders, Elsevier Ltd, 2013. pp. 129–142.
Hwang I, Hahm SC, Choi KA, Park SH, Jeong H, Yea JH, Kim J, Hong S. Intrathecal transplantation of embryonic stem cell-derived spinal GABAergic neural precursor cells attenuates neuropathic pain in a spinal cord injury rat model. Cell Transplant 2016;25:593–607.
Koltzenburg M, Lundberg LE, Torebjörk HE. Dynamic and static components of mechanical hyperalgesia in human hairy skin. PAIN 1992;51:207–19.
Kumru H, Soler D, Vidal J, Tormos JM, Pascual-Leone A, Valls-Sole J. Evoked potentials and quantitative thermal testing in spinal cord injury patients with chronic neuropathic pain. Clin Neurophysiol 2012;123:598–604.
Le Bars D. The whole body receptive field of multireceptive neurones. Prog Brain Res 2002;40:29–44.
Levitan Y, Zeilig G, Bondi M, Ringler E, Defrin R. Predicting the risk for central pain using the sensory components of the international standards for neurological classification of spinal cord injury. J Neurotrauma 2015;32:1684–92.
Maixner W, Dubner R, Kenshalo DR Jr, Bushnell MC, Oliveras JL. Responses of monkey medullary dorsal horn neurons during the detection of noxious heat stimuli. J Neurophysiol 1989;62:437–49.
Margot-Duclot A, Tournebise H, Ventura M, Fattal C. What are the risk factors of occurrence and chronicity of neuropathic pain in spinal cord injury patients? Ann Phys Rehabil Med 2009;52:111–23.
Mehta S, McIntyre A, Janzen S, Loh E, Teasell R. Spinal cord injury rehabilitation evidence team. Systematic review of pharmacologic treatments of pain after spinal cord injury: an update. Arch Phys Med Rehabil 2016;97:1381–91.
Melzack R. The McGill Pain Questionnaire: major properties and scoring methods. PAIN 1975;1:277–99.
Merskey H, Bogduk N. Classification of chronic pain, description of chronic pain syndromes and definitions of pain terms. Seattle: IASP Press, 1994.
Peterson CB, Bogomolov M, Benjamini Y, Sabatti C. Many phenotypes without many false discoveries: error controlling strategies for multitrait association studies. Genet Epidemiol 2016;40:45–56.
Roh DH, Yoon SY, Seo HS, Kang SY, Han HJ, Beitz AJ, Lee JH. Intrathecal injection of carbenoxolone, a gap junction decoupler, attenuates the induction of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 2010;224:123–32.
Siddall PJ, Taylor DA, McClelland JM, Rutkowski SB, Cousins MJ. Pain report and the relationship of pain to physical factors in the first 6 months following spinal cord injury. PAIN 1999;81:187–97.
Siddall PJ, McClelland JM, Rutkowski SB, Cousins MJ. A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. PAIN 2003;103:249–57.
Siddall PJ, Middleton JW. Spinal cord injury-induced pain: mechanisms and treatments. Pain Manag 2015;5:493–507.
Staud R, Robinson ME, Price DD. Temporal summation of second pain and its maintenance are useful for characterizing widespread central sensitization of fibromyalgia patients. J Pain 2007;8:893–901.
Tateda S, Kanno H, Ozawa H, Sekiguchi A, Yahata K, Yamaya S, Itoi E. Rapamycin suppresses microglial activation and reduces the development of neuropathic pain after spinal cord injury. J Orthop Res 2017;35:93–103.
Taylor J, Huelbes S, Albu S, Gómez-Soriano J, Peñacoba C, Poole HM. Neuropathic pain intensity, unpleasantness, coping strategies, and psychosocial factors after spinal cord injury: an exploratory longitudinal study during the first year. Pain Med 2012;13:1457–68.
Teasell RW, Mehta S, Aubut JA, Foulon B, Wolfe DL, Hsieh JT, Townson AF, Short C; Spinal Cord Injury Rehabilitation Evidence Research Team. A systematic review of pharmacologic treatments of pain after spinal cord injury. Arch Phys Med Rehabil 2010;91:816–31.
Treede RD. The role of quantitative sensory testing in the prediction of chronic pain. PAIN 2019;160(suppl 1):S66–9.
Vuckovic A, Jajrees M, Purcell M, Berry H, Fraser M. Electroencephalographic predictors of neuropathic pain in subacute spinal cord injury. J Pain 2018;19:1256.e1–1256.e17.
Wang G, Thompson SM. Maladaptive homeostatic plasticity in a rodent model of central pain syndrome: thalamic hyperexcitability after spinothalamic tract lesions. J Neurosci 2008;28:11959–69.
Warner FM, Cragg JJ, Jutzeler CR, Finnerup NB, Werhagen L, Weidner N, Maier D, Kalke YB, Curt A, Kramer JLK. Progression of neuropathic pain after acute spinal cord injury: a meta-analysis and framework for clinical trials. J Neurotrauma 2019;36:1461–68.
Wasner G, Lee BB, Engel S, McLachlan E. Residual spinothalamic tract pathways predict development of central pain after spinal cord injury. Brain 2008;131:2387–400.
Watanabe S, Uchida K, Nakajima H, Matsuo H, Sugita D, Yoshida A, Honjoh K, Johnson WE, Baba H. Early transplantation of mesenchymal stem cells after spinal cord injury relieves pain hypersensitivity through suppression of pain-related signaling cascades and reduced inflammatory cell recruitment. Stem Cells 2015;33:1902–14.
Widerström-Noga E, Biering-Sørensen F, Bryce T, Cardenas DD, Finnerup NB, Jensen MP, Richards JS, Siddall PJ. The international spinal cord injury pain basic data set. Spinal Cord 2008;46:818–23.
Widerström-Noga E, Felix ER, Adcock JP, Escalona M, Tibbett J. Multidimensional neuropathic pain phenotypes after spinal cord injury. J Neurotrauma 2016;33:482–92.
Wu J, Zhao Z, Zhu X, Renn CL, Dorsey SG, Faden AI. Cell cycle inhibition limits development and maintenance of neuropathic pain following spinal cord injury. PAIN 2016;157:488–503.
Wydenkeller S, Maurizio S, Dietz V, Halder P. Neuropathic pain in spinal cord injury: significance of clinical and electrophysiological measures. Eur J Neurosci 2009;30:91–9.
Yarnitsky D, Arendt-Nielsen L, Bouhassira D, Edwards RR, Fillingim RB, Granot M, Hansson P, Lautenbacher S, Marchand S, Wilder-Smith O. Recommendations on terminology and practice of psychophysical DNIC testing. Eur J Pain 2010;14:339.
Yarnitsky D, Granot M, Granovsky Y. Pain modulation profile and pain therapy: between pro- and antinociception. PAIN 2014;155:663–5.
Zeilig G, Enosh S, Rubin-Asher D, Lehr B, Defrin R. The nature and course of sensory changes following spinal cord injury: predictive properties and implications on the mechanism of central pain. Brain 2012;135:418–30.