Early afferent activity from the facet joint after painful trauma to its capsule potentiates neuronal excitability and glutamate signaling in the spinal cord

Pain

Volumn 155, Issue 9, 2014, Pages 1878-1887

  Crosby, Nathan D ^a   Gilliland, Taylor M ^a   Winkelstein, Beth A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bupivacaine; Facet joint; Glutamate; Hyperalgesia; Neuronal hyperexcitability; Pain

Indexed keywords

BUPIVACAINE; EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; METABOTROPIC RECEPTOR 5; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PROTEIN; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; CERVICAL FACET JOINT INJURY; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; DRUG EFFICACY; GENE SILENCING; HYPERALGESIA; MALE; NERVE CELL; NERVE CELL EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SENSITIZATION; SHAM PROCEDURE; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; ANIMAL; DOWN REGULATION; INJURIES; METABOLISM; PAIN MEASUREMENT; PATHOPHYSIOLOGY; PHYSIOLOGY; SENSORY NERVE CELL; UPREGULATION; ZYGAPOPHYSEAL JOINT;

ANIMALS; DOWN-REGULATION; GLUTAMIC ACID; HYPERALGESIA; MALE; NEURONS, AFFERENT; PAIN MEASUREMENT; RATS; SIGNAL TRANSDUCTION; SPINAL CORD; UP-REGULATION; ZYGAPOPHYSEAL JOINT;

EID: 84926418381     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.06.019     Document Type: Article

References (64)

1. Araujo MC, Sinnott CJ, Strichartz GR. Multiple phases of relief from experimental mechanical allodynia by systemic lidocaine: responses to early and late infusions. PAIN 2003;103:21-9.
2. Barnsley L, Bogduk N. Medial branch blocks are specific for the diagnosis of cervical zygapophyseal joint pain. Region Anesth 1993;18:343-50.
3. Barnsley L, Lord SM, Wallis BJ, Bogduk N. The prevalence of chronic cervical zygapophysial joint pain after whiplash. Spine 1995;20:20-6.
4. Benveniste EN. Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action. Am J Physiol 1992;263:C1-C16.
5. Brenner GJ, Ji RR, Shaffer S, Woolf CJ. Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. Eur J Neurosci 2004;20:375-84.
6. Chen C, Lu Y, Kallakuri S, Patwardhan A, Cavanaugh JM. Distribution of A-delta and C-fiber receptors in the cervical facet joint capsule and their response to stretch. J Bone Joint Surg 2006;88:1807-16.
7. Chen DW, Hu CC, Chang YH, Lee MS, Chang CJ, Hsieh PH. Intra-articular bupivacaine reduces postoperative pain and meperidine use after total hip arthroplasty: a randomized double-blind study. J Arthroplasty (in press).
8. Chen L, Huang LM. Protein kinase C reduces Mg2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 1992;356:521-3.
9. Christensen MD, Hulsebosch CE. Chronic central pain after spinal cord injury. J Neurotraum 1997;14:517-37.
10. Cook AJ, Woolf CJ, Wall PD, McMahon SB. Dynamic receptive field plasticity in rat spinal cord dorsal horn following C-primary afferent input. Nature 1987;325:151-3.
11. Crosby ND, Weisshaar CL, Winkelstein BA. Spinal neuronal plasticity is evident within 1 day after a painful cervical facet joint injury. Neurosci Lett 2013;542:102-6.
12. Danbolt NC. Glutamate uptake. Prog Neurobiol 2001;65:1-105.
13. Devor M. Ectopic discharge in A-beta afferents as a source of neuropathic pain. Exp Brain Res 2009;196:115-28.
14. Dingledine R, Borges K, Bowie D, Traynelis SF. The glutamate receptor ion channels. Pharmacol Rev 1999;51:7-62.
15. Djouhri L, Koutsikou S, Fang X, McMullan S, Lawson SN. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. Neurobiol Dis 2006;26:1281-92.
16. Dong L, Quindlen JC, Lipschutz DE, Winkelstein BA. Whiplash-like facet joint loading initiates glutamatergic responses in the DRG and spinal cord associated with behavioral hypersensitivity. Brain Res 2012;1461:51-63.
17. Dong L, Winkelstein BA. Simulated whiplash modulates expression of the glutamatergic system in the spinal cord suggesting spinal plasticity is associated with painful dynamic cervical facet loading. J Neurotraum 2010;27:163-74.
18. Dyhre H, Lang M, Wallin R, Renck H. The duration of action of bupivacaine, levobupivacaine, ropivacaine and pethidine in peripheral nerve block in the rat. Acta Anaesthesiol Scand 1997;41:1346-52.
19. Gissen AJ, Covino BG, Gregus J. Differential sensitivity of fast and slow fibers in mammalian nerve: effect of etidocaine and bupivacaine on fast/slow fibers. Anesth Analg 1982;61:570-5.
20. Gonzales-Darder JM, Barbera J, Abellan MJ. Effect of prior anesthesia on autotomy following sciatic transection in rats. PAIN 1986;24:87-91.
21. Hains BC, Klein JP, Saab CY, Craner MJ, Black JA, Waxman SG. Upregulation of sodium channel Nav1.3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci 2003;23:8881-92.
22. Herren-Gerber R, Weiss S, Arendt-Nielsen L, Petersen-Felix S, Di Stefano G, Radanov BP, Curatolo M. Modulation of central hypersensitivity by nociceptive input in chronic pain after whiplash injury. Pain Med 2004;5:366-76.
23. Hogg-Johnson S, van der Velde G, Carroll LJ, Holm LW, Cassidy JD, Guzman J, Cote P, Haldeman S, Ammendolia C, Carragee E, Hurwitz E, Nordin M, Peloso P. The burden and determinants of neck pain in the general population. Eur Spine J 2008;17:S39-51.
24. Kallakuri S, Singh A, Chen C, Cavanaugh JM. Demonstration of substance P, calcitonin gene-related peptide, and protein gene product 9.5 containing nerve fibers in human cervical facet joint capsules. Spine 2004;29:1182-6.
25. Kallakuri S, Singh A, Lu Y, Chen C, Patwardhan A, Cavanaugh JM. Tensile stretching of cervical facet joint capsule and related axonal changes. Eur Spine J 2008;17:556-63.
26. Kawasaki Y, Kohno T, Zhuang ZY, Brenner GJ, Wang H, Ven Der Meer C, Befort K, Woolf CJ, Ji RR. Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci 2004;24:8310-21.
27. Kiyatkin A, Aksamitiene E. Multistrip Western blotting to increase quantitative data output. Methods Mol Biol 2009;536:149-61.
28. Klein SM, Greengrass RA, Steele SM, D'Ercole FJ, Speer KP, Gleason DH, DeLong ER, Warner DS. A comparison of 0.5% bupivacaine, 0.5% ropivacaine, and 0.75% ropivacaine for interscalene brachial plexus block. Anesth Analg 1998;87:1316-9.
29. Kras JV, Tanaka K, Gilliland TM, Winkelstein BA. An anatomical and immunohistochemical characterization of afferents innervating the C6/C7 facet joint after painful joint loading in the rat. Spine 2013;38:E325-31.
30. Kras JV, Dong L, Winkelstein BA. Increased interleukin-1 & prostaglandin E2 expression in the spinal cord at day 1 after painful facet joint injury: evidence of early spinal inflammation. Spine 2014;39:207-12.
31. Lander P. Selective cervical nerve blocks. In: Schweitzer ME, Laredo JD, editors. New techniques in interventional musculoskeletal radiology. New York: Informa Healthcare; 2007.
32. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009;10:895-926.
33. Lee KE, Davis MB, Mejilla RM, Winkelstein BA. In vivo cervical facet capsule distraction: mechanical implications for whiplash & neck pain. Stapp Car C 2004;48:373-96.
34. Lee KE, Davis MB, Winkelstein BA. Capsular ligament involvement in the development of mechanical hyperalgesia after facet joint loading: behavioral and inflammatory outcomes in a rodent model of pain. J Neurotraum 2008;25:1383-93.
35. Lee KE, Winkelstein BA. Joint distraction magnitude is associated with different behavioral outcomes and substance P levels for cervical facet joint loading in the rat. J Pain 2009;10:436-45.
36. Lin SC, Yeh JH, Chen CL, Chou SH, Tsai YJ. Effects of local lidocaine treatment before and after median nerve injury on mechanical hypersensitivity and microglia activation in rat cuneate nucleus. Eur J Pain 2011;15:359-67.
37. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, Devor M. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. PAIN 2000;85:203-521.
38. Lord SM, Barnsley L, Wallis BJ, Bogduk N. Chronic cervical zygapophysial joint pain after whiplash: A placebo-controlled prevalence study. Spine 1996;21:1737-44.
39. Lord SM, Barnsley L, Wallis BJ, McDonald GJ, Bogduk N. Percutaneous radiofrequency neurotomy for chronic cervical zygapophyseal-joint pain. N Engl J Med 1996;335:1721-6.
40. Lu Y, Chen C, Kallakuri S, Patwardhan A, Cavanaugh JM. Neural response of cervical facet joint capsule to stretch: a study of whiplash pain mechanisms. Stapp Car C 2005;49:49-65.
41. Manchikanti L, Boswell MV, Singh V, Pampati V, Damron KS, Beyer CD. Prevalence of facet joint pain in chronic spinal pain of cervical, thoracic, and lumbar regions. BMC Musculoskelet Disord 2004;5:15.
42. Manchikanti L, Singh V, Falco FJE, Cash KM, Fellows B. Cervical medial branch blocks for chronic cervical facet joint pain. Spine 2008;33:1813-20.
43. Mayer ML, Westbrook GL, Guthrie PB. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurons. Nature 1984;309:261-3.
44. McLain RF. Mechanoreceptor endings in human cervical facet joints. Spine 1994;19:495-501.
45. Pekny M, Nilsson M. Astrocyte activation and reactive gliosis. Glia 2005;50:427-34.
46. Quinn KP, Dong L, Golder FJ, Winkelstein BA. Neuronal hyperexcitability in the dorsal horn after painful facet joint injury. PAIN 2010;151:414-21.
47. Ramos KM, Lewis MT, Morgan KN, Crysdale NY, Kroll JL, Taylor FR, Harrison JA, Sloane EM, Maier SF, Watkins LR. Spinal upregulation of glutamate transporter GLT-1 by ceftriaxone: therapeutic efficacy in a range of experimental nervous system disorders. Neuroscience 2010;169:1888-900.
48. Roy DF, Fleury J, Fontaine SB, Dussault RG. Clinical evaluation of cervical facet joint infiltration. J Can Assoc Radiol 1988;39:118-20.
49. Seltzer Z, Beilin B, Ginzburg R, Paran Y, Shimko T. The role of injury discharge in the induction of neuropathic pain behavior in rats. PAIN 1991;46:327-36.
50. Seltzer Z, Cohn S, Ginzburg R, Beilin B. Modulation of neuropathic pain behavior in rats by spinal disinhibition and NMDA receptor blockade of injury discharge. PAIN 1991;45:69-75.
51. Shankarappa SA, Tsui JH, Kim KN, Reznor G, Dohlman JG, Langer R, Kohane DS. Prolonged nerve blockade delays the onset of neuropathic pain. Proc Natl Acad Sci U S A 2012;109:17555-60.
52. Tabatabai M, Booth AM. Mechanism of action of local anesthetics on synaptic transmission in the rat. Anesth Analg 1990;71:149-57.
53. Wall PD, Woolf CJ. The brief and the prolonged facilitatory effects of unmyelinated afferent input on the rat spinal cord are independently influenced by peripheral nerve section. Neuroscience 1986;17:1199-205.
54. Watkins LR, Milligan ED, Maier SF. Glial activation: a driving force for pathological pain. Trends Neurosci 2001;24:450-5.
55. Wei J, Yang HB, Qin JB, Kong FJ, Yang TB. Single-dose intra-articular bupivacaine after knee arthroscopic surgery: a meta-analysis of randomized placebo-controlled studies. Knee Surg Sports Traumatol Arthrosc 2014;22:1517-28.
56. Weisshaar CL, Dong L, Bowman AS, Perez FM, Guarino BB, Sweitzer SM, Winkelstein BA. Metabotropic glutamate receptor-5 and protein kinase Cepsilon increase in dorsal root ganglion neurons and spinal glial activation in an adolescent rat model of painful neck injury. J Neurotrauma 2010;27:2261-71.
57. Weisshaar CL, Winkelstein BA. Ablating spinal NK1-bearing neurons eliminates the development of pain and reduces spinal neuronal hyperexcitability and inflammation from mechanical joint injury in the rat. J Pain 2014;15:378-86.
58. Winkelstein BA, Santos DG. An intact facet capsular ligament modulates behavioral sensitivity and spinal glial activation produced by cervical facet joint tension. Spine 2008;33:856-62.
59. Woolf CJ, Chong MS. Preemptive analgesia-treating postoperative pain by preventing the establishment of central sensitization. Anesth Analg 1993;77:362-79.
60. Xie W, Strong JA, Meij JTA, Zhang JM, Yu L. Neuropathic pain: early spontaneous afferent activity is the trigger. PAIN 2005;116:243-56.
61. Yamashita T, Cavanaugh JM, el-Bohy AA, Getchell TV, King AI. Mechanosensitive afferent units in the lumbar facet joint. J Bone Joint Surg Am 1990;72:865-70.
62. Yang F, Whang J, Derry WT, Vardeh D, Scholz J. Analgesic treatment with pregabalin does not prevent persistent pain after peripheral nerve injury in the rat. PAIN 2014;155:356-66.
63. Zhang H, Xie W, Xie Y. Spinal cord injury triggers sensitization of wide dynamic range dorsal horn neurons in segments rostral to the injury. Brain Res 2005;1055:103-10.
64. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. PAIN 1983;16:109-10.