Behavioral characterization and effect of clinical drugs in a rat model of pain following spinal cord compression

Brain Research

Volumn 1185, Issue 1, 2007, Pages 117-128

  Hama, Aldric ^a   Sagen, Jacqueline ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Allodynia; Analgesia; Clinical translation; Hyperalgesia; Pain; Spinal cord injury

Indexed keywords

AMITRIPTYLINE; BACLOFEN; CARBAMAZEPINE; DIAZEPAM; GABAPENTIN; MEMANTINE; MORPHINE; ROFECOXIB; TRAMADOL;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC PAIN; CLIP; CONTROLLED STUDY; COOLING; DISEASE MODEL; HARGREAVES TEST; HEATING; HINDLIMB; HYPERALGESIA; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; RELIABILITY; SPINAL CORD COMPRESSION; SPRAGUE DAWLEY RAT; SYMPTOM; VON FREY FILAMENT;

ANALGESICS; ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SPINAL CORD COMPRESSION; TIME FACTORS;

RATTUS;

EID: 36448959087     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.09.013     Document Type: Article

References (97)

1. Ahn S.H., Park H.W., Lee B.S., Moon H.W., Jang S.H., Sakong J., and Bae J.H. Gabapentin effect on neuropathic pain compared among patients with spinal cord injury and different durations of symptoms. Spine 28 (2003) 341-346 (discussion 346-347)
2. Attal N., Rouaud J., Brasseur L., Chauvin M., and Bouhassira D. Systemic lidocaine in pain due to peripheral nerve injury and predictors of response. Neurology 62 (2004) 218-225
3. Backonja M., and Glanzman R.L. Gabapentin dosing for neuropathic pain: evidence from randomized, placebo-controlled clinical trials. Clin. Ther. 25 (2003) 81-104
4. Basso D.M., Beattie M.S., and Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12 (1995) 1-21
5. Bennett G., Serafini M., Burchiel K., Buchser E., Classen A., Deer T., Du Pen S., Ferrante F.M., Hassenbusch S.J., Lou L., Maeyaert J., Penn R., Portenoy R.K., Rauck R., Willis K.D., and Yaksh T. Evidence-based review of the literature on intrathecal delivery of pain medication. J. Pain Symptom Manage. 20 (2000) S12-S36
6. Beric A., Dimitrijevic M.R., and Lindblom U. Central dysesthesia syndrome in spinal cord injury patients. Pain 34 (1988) 109-116
7. Blackburn-Munro G. Pain-like behaviours in animals-how human are they?. Trends Pharmacol. Sci. 25 (2004) 299-305
8. Brodkin J., Busse C., Sukoff S.J., and Varney M.A. Anxiolytic-like activity of the mGluR5 antagonist MPEP a comparison with diazepam and buspirone. Pharmacol. Biochem. Behav. 73 (2002) 359-366
9. Bruce J.C., Oatway M.A., and Weaver L.C. Chronic pain after clip-compression injury of the rat spinal cord. Exp. Neurol. 178 (2002) 33-48
10. Bunge R.P., Puckett W.R., Becerra J.L., Marcillo A., and Quencer R.M. Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv. Neurol. 59 (1993) 75-89
11. Cardenas D.D., Warms C.A., Turner J.A., Marshall H., Brooke M.M., and Loeser J.D. Efficacy of amitriptyline for relief of pain in spinal cord injury: results of a randomized controlled trial. Pain 96 (2002) 365-373
12. Chan C.C., Boyce S., Brideau C., Charleson S., Cromlish W., Ethier D., Evans J., Ford-Hutchinson A.W., Forrest M.J., Gauthier J.Y., Gordon R., Gresser M., Guay J., Kargman S., Kennedy B., Leblanc Y., Leger S., Mancini J., O'Neill G.P., Ouellet M., Patrick D., Percival M.D., Perrier H., Prasit P., Rodger I., et al. Rofecoxib [Vioxx, MK-0966; 4-(4′-methylsulfonylphenyl)-3-phenyl-2-(5H)-furanone]: a potent and orally active cyclooxygenase-2 inhibitor. Pharmacological and biochemical profiles. J. Pharmacol. Exp. Ther. 290 (1999) 551-560
13. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53 (1994) 55-63
14. Chiou-Tan F.Y., Tuel S.M., Johnson J.C., Priebe M.M., Hirsh D.D., and Strayer J.R. Effect of mexiletine on spinal cord injury dysesthetic pain. Am. J. Phys. Med. Rehabil. 75 (1996) 84-87
15. Choi Y., Yoon Y.W., Na H.S., Kim S.H., and Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59 (1994) 369-376
16. Davidoff G., Guarracini M., Roth E., Sliwa J., and Yarkony G. Trazodone hydrochloride in the treatment of dysesthetic pain in traumatic myelopathy: a randomized, double-blind, placebo-controlled study. Pain 29 (1987) 151-161
17. de Felipe M.C., de Ceballos M.L., and Fuentes J.A. Hypoalgesia induced by antidepressants in mice: a case for opioids and serotonin. Eur. J. Pharmacol. 125 (1986) 193-199
18. De Vry J., Kuhl E., Franken-Kunkel P., and Eckel G. Pharmacological characterization of the chronic constriction injury model of neuropathic pain. Eur. J. Pharmacol. 491 (2004) 137-148
19. Dellemijn P.L., and Vanneste J.A. Randomised double-blind active-placebo-controlled crossover trial of intravenous fentanyl in neuropathic pain. Lancet 349 (1997) 753-758
20. Deumens R., Koopmans G.C., and Joosten E.A. Regeneration of descending axon tracts after spinal cord injury. Prog. Neurobiol. 77 (2005) 57-89
21. Eaton M.J., Martinez M.A., and Karmally S. A single intrathecal injection of GABA permanently reverses neuropathic pain after nerve injury. Brain Res. 835 (1999) 334-339
22. Eide P.K. Pathophysiological mechanisms of central neuropathic pain after spinal cord injury. Spinal Cord 36 (1998) 601-612
23. Eide P.K., Jorum E., and Stenehjem A.E. Somatosensory findings in patients with spinal cord injury and central dysaesthesia pain. J. Neurol. Neurosurg. Psychiatry 60 (1996) 411-415
24. Eisenberg E., LaCross S., and Strassman A.M. The clinically tested N-methyl-d-aspartate receptor antagonist memantine blocks and reverses thermal hyperalgesia in a rat model of painful mononeuropathy. Neurosci. Lett. 187 (1995) 17-20
25. Eisenberg E., Kleiser A., Dortort A., Haim T., and Yarnitsky D. The NMDA (N-methyl-d-aspartate) receptor antagonist memantine in the treatment of postherpetic neuralgia: a double-blind, placebo-controlled study. Eur. J. Pain 2 (1998) 321-327
26. Erichsen H.K., and Blackburn-Munro G. Pharmacological characterisation of the spared nerve injury model of neuropathic pain. Pain 98 (2002) 151-161
27. Erichsen H.K., Hao J.X., Xu X.J., and Blackburn-Munro G. Comparative actions of the opioid analgesics morphine, methadone and codeine in rat models of peripheral and central neuropathic pain. Pain 116 (2005) 347-358
28. Esser M.J., and Sawynok J. Acute amitriptyline in a rat model of neuropathic pain: differential symptom and route effects. Pain 80 (1999) 643-653
29. Finnerup N.B., and Jensen T.S. Spinal cord injury pain-mechanisms and treatment. Eur. J. Neurol. 11 (2004) 73-82
30. Finnerup N.B., Johannesen I.L., Sindrup S.H., Bach F.W., and Jensen T.S. Pain and dysesthesia in patients with spinal cord injury: a postal survey. Spinal Cord 39 (2001) 256-262
31. Finnerup N.B., Gyldensted C., Nielsen E., Kristensen A.D., Bach F.W., and Jensen T.S. MRI in chronic spinal cord injury patients with and without central pain. Neurology 61 (2003) 1569-1575
32. Finnerup N.B., Biering-Sorensen F., Johannesen I.L., Terkelsen A.J., Juhl G.I., Kristensen A.D., Sindrup S.H., Bach F.W., and Jensen T.S. Intravenous lidocaine relieves spinal cord injury pain: a randomized controlled trial. Anesthesiology 102 (2005) 1023-1030
33. Finnerup N.B., Sorensen L., Biering-Sorensen F., Johannesen I.L., and Jensen T.S. Segmental hypersensitivity and spinothalamic function in spinal cord injury pain. Exp. Neurol. 207 (2007) 139-149
34. Fox A., Gentry C., Patel S., Kesingland A., and Bevan S. Comparative activity of the anti-convulsants oxcarbazepine, carbamazepine, lamotrigine and gabapentin in a model of neuropathic pain in the rat and guinea-pig. Pain 105 (2003) 355-362
35. Franklin K.B., and Abbott F.V. Pentobarbital, diazepam, and ethanol abolish the interphase diminution of pain in the formalin test: evidence for pain modulation by GABAA receptors. Pharmacol. Biochem. Behav. 46 (1993) 661-666
36. Gerke M.B., Duggan A.W., Xu L., and Siddall P.J. Thalamic neuronal activity in rats with mechanical allodynia following contusive spinal cord injury. Neuroscience 117 (2003) 715-722
37. Geyer M.A., and Markou A. Animal models of psychiatric disorders. In: Bloom F.E., and Kupfer D.J. (Eds). Psychopharamacology: The Fourth Generation of Progress (1995), Raven Press, New York 787-798
38. Ghelardini C., Galeotti N., and Bartolini A. Antinociception induced by amitriptyline and imipramine is mediated by alpha2A-adrenoceptors. Jpn. J. Pharmacol. 82 (2000) 130-137
39. Goff J.R., Burkey A.R., Goff D.J., and Jasmin L. Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behaviour. Neuroscience 82 (1998) 559-574
40. Gracely R.H., Dubner R., and McGrath P.A. Fentanyl reduces the intensity of painful tooth pulp sensations: controlling for detection of active drugs. Anesth. Analg. 61 (1982) 751-755
41. Guneli E., Karabay Yavasoglu N.U., Apaydin S., Uyar M., and Uyar M. Analysis of the antinociceptive effect of systemic administration of tramadol and dexmedetomidine combination on rat models of acute and neuropathic pain. Pharmacol. Biochem. Behav. 88 (2007) 9-17
42. Gwak Y.S., Tan H.Y., Nam T.S., Paik K.S., Hulsebosch C.E., and Leem J.W. Activation of spinal GABA receptors attenuates chronic central neuropathic pain after spinal cord injury. J. Neurotrauma 23 (2006) 1111-1124
43. Hains B.C., Yucra J.A., and Hulsebosch C.E. Reduction of pathological and behavioral deficits following spinal cord contusion injury with the selective cyclooxygenase-2 inhibitor NS-398. J. Neurotrauma 18 (2001) 409-423
44. Hains B.C., Everhart A.W., Fullwood S.D., and Hulsebosch C.E. Changes in serotonin, serotonin transporter expression and serotonin denervation supersensitivity: involvement in chronic central pain after spinal hemisection in the rat. Exp. Neurol. 175 (2002) 347-362
45. Hama A., Woon Lee J., and Sagen J. Differential efficacy of intrathecal NMDA receptor antagonists on inflammatory mechanical and thermal hyperalgesia in rats. Eur. J. Pharmacol. 459 (2003) 49-58
46. Hao J.X., and Xu X.J. Treatment of a chronic allodynia-like response in spinally injured rats: effects of systemically administered excitatory amino acid receptor antagonists. Pain 66 (1996) 279-285
47. Hao J.X., Xu X.J., Aldskogius H., Seiger A., and Wiesenfeld-Hallin Z. Allodynia-like effects in rat after ischaemic spinal cord injury photochemically induced by laser irradiation. Pain 45 (1991) 175-185
48. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
49. Herman R.M., D'Luzansky S.C., and Ippolito R. Intrathecal baclofen suppresses central pain in patients with spinal lesions. A pilot study. Clin. J. Pain 8 (1992) 338-345
50. Hofstetter C.P., Holmstrom N.A., Lilja J.A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S.N., Frisen J., and Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci. 8 (2005) 346-353
51. Hunter J.C., Gogas K.R., Hedley L.R., Jacobson L.O., Kassotakis L., Thompson J., and Fontana D.J. The effect of novel anti-epileptic drugs in rat experimental models of acute and chronic pain. Eur. J. Pharmacol. 324 (1997) 153-160
52. Ibuki T., Hama A.T., Wang X.T., Pappas G.D., and Sagen J. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 76 (1997) 845-858
53. Jett M.F., McGuirk J., Waligora D., and Hunter J.C. The effects of mexiletine, desipramine and fluoxetine in rat models involving central sensitization. Pain 69 (1997) 161-169
54. Kakulas B.A. The clinical neuropathology of spinal cord injury. A guide to the future. Paraplegia 25 (1987) 212-216
55. Kastin A.J., and Pan W. Targeting neurite growth inhibitors to induce CNS regeneration. Curr. Pharm. Des. 11 (2005) 1247-1253
56. Korzeniewska-Rybicka I., and Plaznik A. Analgesic effect of antidepressant drugs. Pharmacol. Biochem. Behav. 59 (1998) 331-338
57. Krumins S.A., and Faden A.I. Traumatic injury alters opiate receptor binding in rat spinal cord. Ann. Neurol. 19 (1986) 498-501
58. Kulbatski I., Mothe A.J., Nomura H., and Tator C.H. Endogenous and exogenous CNS derived stem/progenitor cell approaches for neurotrauma. Curr. Drug Targets 6 (2005) 111-126
59. Kvarnstrom A., Karlsten R., Quiding H., and Gordh T. The analgesic effect of intravenous ketamine and lidocaine on pain after spinal cord injury. Acta Anaesthesiol. Scand. 48 (2004) 498-506
60. Lampert A., Hains B.C., and Waxman S.G. Upregulation of persistent and ramp sodium current in dorsal horn neurons after spinal cord injury. Exp. Brain Res. 174 (2006) 660-666
61. Lee Y.W., Chaplan S.R., and Yaksh T.L. Systemic and supraspinal, but not spinal, opiates suppress allodynia in a rat neuropathic pain model. Neurosci. Lett. 199 (1995) 111-114
62. Levendoglu F., Ogun C.O., Ozerbil O., Ogun T.C., and Ugurlu H. Gabapentin is a first line drug for the treatment of neuropathic pain in spinal cord injury. Spine 29 (2004) 743-751
63. Luo Z.D., Chaplan S.R., Higuera E.S., Sorkin L.S., Stauderman K.A., Williams M.E., and Yaksh T.L. Upregulation of dorsal root ganglion (alpha)2(delta) calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J. Neurosci. 21 (2001) 1868-1875
64. Ma Y., Feigin A., Dhawan V., Fukuda M., Shi Q., Greene P., Breeze R., Fahn S., Freed C., and Eidelberg D. Dyskinesia after fetal cell transplantation for parkinsonism: a PET study. Ann. Neurol. 52 (2002) 628-634
65. Malonne H., Coffiner M., Fontaine D., Sonet B., Sereno A., Peretz A., and Vanderbist F. Long-term tolerability of tramadol LP, a new once-daily formulation, in patients with osteoarthritis or low back pain. J. Clin. Pharm. Ther. 30 (2005) 113-120
66. McQuay H., Carroll D., Jadad A.R., Wiffen P., and Moore A. Anticonvulsant drugs for management of pain: a systematic review. BMJ 311 (1995) 1047-1052
67. McQuay H.J., Tramer M., Nye B.A., Carroll D., Wiffen P.J., and Moore R.A. A systematic review of antidepressants in neuropathic pain. Pain 68 (1996) 217-227
68. Medvedev I.O., Malyshkin A.A., Belozertseva I.V., Sukhotina I.A., Sevostianova N.Y., Aliev K., Zvartau E.E., Parsons C.G., Danysz W., and Bespalov A.Y. Effects of low-affinity NMDA receptor channel blockers in two rat models of chronic pain. Neuropharmacology 47 (2004) 175-183
69. Millan M.J. The induction of pain: an integrative review. Prog. Neurobiol. 57 (1999) 1-164
70. Mills C.D., Grady J.J., and Hulsebosch C.E. Changes in exploratory behavior as a measure of chronic central pain following spinal cord injury. J. Neurotrauma 18 (2001) 1091-1105
71. Mills C.D., Hains B.C., Johnson K.M., and Hulsebosch C.E. Strain and model differences in behavioral outcomes after spinal cord injury in rat. J. Neurotrauma 18 (2001) 743-756
72. Monasky M.S., Zinsmeister A.R., Stevens C.W., and Yaksh T.L. Interaction of intrathecal morphine and ST-91 on antinociception in the rat: dose-response analysis, antagonism and clearance. J. Pharmacol. Exp. Ther. 254 (1990) 383-392
73. Nicholson B.D. Evaluation and treatment of central pain syndromes. Neurology 62 (2004) S30-S36
74. Oatway M.A., Chen Y., and Weaver L.C. The 5-HT3 receptor facilitates at-level mechanical allodynia following spinal cord injury. Pain 110 (2004) 259-268
75. Ozaki S., Narita M., Narita M., Iino M., Sugita J., Matsumura Y., and Suzuki T. Suppression of the morphine-induced rewarding effect in the rat with neuropathic pain: implication of the reduction in mu-opioid receptor functions in the ventral tegmental area. J. Neurochem. 82 (2002) 1192-1198
76. Patel S., Naeem S., Kesingland A., Froestl W., Capogna M., Urban L., and Fox A. The effects of GABA(B) agonists and gabapentin on mechanical hyperalgesia in models of neuropathic and inflammatory pain in the rat. Pain 90 (2001) 217-226
77. Portenoy R.K., Foley K.M., and Inturrisi C.E. The nature of opioid responsiveness and its implications for neuropathic pain: new hypotheses derived from studies of opioid infusions. Pain 43 (1990) 273-286
78. Raffa R.B., Friderichs E., Reimann W., Shank R.P., Codd E.E., and Vaught J.L. Opioid and nonopioid components independently contribute to the mechanism of action of tramadol, an 'atypical' opioid analgesic. J. Pharmacol. Exp. Ther. 260 (1992) 275-285
79. Raffa R.B., Clark-Vetri R., Tallarida R.J., and Wertheimer A.I. Combination strategies for pain management. Expert Opin. Pharmacother. 4 (2003) 1697-1708
80. Ragnarsson K.T. Management of pain in persons with spinal cord injury. J. Spinal Cord Med. 20 (1997) 186-199
81. Resnick D.K., Graham S.H., Dixon C.E., and Marion D.W. Role of cyclooxygenase 2 in acute spinal cord injury. J. Neurotrauma 15 (1998) 1005-1013
82. Riendeau D., Percival M.D., Brideau C., Charleson S., Dube D., Ethier D., Falgueyret J.P., Friesen R.W., Gordon R., Greig G., Guay J., Mancini J., Ouellet M., Wong E., Xu L., Boyce S., Visco D., Girard Y., Prasit P., Zamboni R., Rodger I.W., Gresser M., Ford-Hutchinson A.W., Young R.N., and Chan C.C. Etoricoxib (MK-0663): preclinical profile and comparison with other agents that selectively inhibit cyclooxygenase-2. J. Pharmacol. Exp. Ther. 296 (2001) 558-566
83. Rivlin A.S., and Tator C.H. Effect of duration of acute spinal cord compression in a new acute cord injury model in the rat. Surg. Neurol. 10 (1978) 38-43
84. Siddall P.J., Cousins M.J., Otte A., Griesing T., Chambers R., and Murphy T.K. Pregabalin in central neuropathic pain associated with spinal cord injury: a placebo-controlled trial. Neurology 67 (2006) 1792-1800
85. Sindrup S.H., and Jensen T.S. Efficacy of pharmacological treatments of neuropathic pain: an update and effect related to mechanism of drug action. Pain 83 (1999) 389-400
86. Singh V.P., Patil C.S., and Kulkarni S.K. Analysis of interaction between etoricoxib and tramadol against mechanical hyperalgesia of spinal cord injury in rats. Life Sci. 78 (2006) 1168-1174
87. Stevens C.W., Kajander K.C., Bennett G.J., and Seybold V.S. Bilateral and differential changes in spinal mu, delta and kappa opioid binding in rats with a painful, unilateral neuropathy. Pain 46 (1991) 315-326
88. Stolp-Smith K.A., and Wainberg M.C. Antidepressant exacerbation of spasticity. Arch. Phys. Med. Rehabil. 80 (1999) 339-342
89. Tallarida R.J., and Murray R.B. Manual of Pharmacological Calculations with Computer Programs (1981), Springer-Verlag, New York, NY
90. Tsai Y.C., Sung Y.H., Chang P.J., Kang F.C., and Chu K.S. Tramadol relieves thermal hyperalgesia in rats with chronic constriction injury of the sciatic nerve. Fundam. Clin. Pharmacol. 14 (2000) 335-340
91. Vissers K.C., Geenen F., Biermans R., and Meert T.F. Pharmacological correlation between the formalin test and the neuropathic pain behavior in different species with chronic constriction injury. Pharmacol. Biochem. Behav. 84 (2006) 479-486
92. Wallace M.S., Magnuson S., and Ridgeway B. Efficacy of oral mexiletine for neuropathic pain with allodynia: a double-blind, placebo-controlled, crossover study. Reg. Anesth. Pain Med. 25 (2000) 459-467
93. Widerstrom-Noga E.G., and Turk D.C. Types and effectiveness of treatments used by people with chronic pain associated with spinal cord injuries: influence of pain and psychosocial characteristics. Spinal Cord 41 (2003) 600-609
94. Woolf C.J., Shortland P., and Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355 (1992) 75-78
95. Xu X.J., Hao J.X., Seiger A., Arner S., Lindblom U., and Wiesenfeld-Hallin Z. Systemic mexiletine relieves chronic allodynialike symptoms in rats with ischemic spinal cord injury. Anesth. Analg. 74 (1992) 649-652
96. Yezierski R.P., Liu S., Ruenes G.L., Kajander K.J., and Brewer K.L. Excitotoxic spinal cord injury: behavioral and morphological characteristics of a central pain model. Pain 75 (1998) 141-155
97. Zhang A.L., Hao J.X., Seiger A., Xu X.J., Wiesenfeld-Hallin Z., Grant G., and Aldskogius H. Decreased GABA immunoreactivity in spinal cord dorsal horn neurons after transient spinal cord ischemia in the rat. Brain Res. 656 (1994) 187-190