A novel model of combined neuropathic and inflammatory pain displaying long-lasting allodynia and spontaneous pain-like behaviour

Neuroscience Research

Volumn 74, Issue 3-4, 2012, Pages 230-238

  Allchorne, Andrew J ^a   Gooding, Hayley L ^a   Mitchell, Rory ^a   Fleetwood Walker, Sue M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Analgesia; Inflammatory; Neuropathic; Pain behaviour; Spontaneous pain

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; DICLOFENAC; FREUND ADJUVANT; GABAPENTIN; MEXILETINE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; DRUG EFFICACY; HYPERALGESIA; INFLAMMATORY PAIN; MALE; NEUROPATHIC PAIN; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; STATISTICAL SIGNIFICANCE;

ACTIVATING TRANSCRIPTION FACTOR 3; ADJUVANTS, IMMUNOLOGIC; ANIMALS; BEHAVIOR, ANIMAL; CHRONIC PAIN; DISEASE MODELS, ANIMAL; FREUND'S ADJUVANT; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NEURALGIA; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE;

EID: 84871934044     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2012.10.006     Document Type: Article

References (50)

1. Akada Y., Ogawa S., Amano K., Fukudome Y., Yamasaki F., Itoh M., Yamamoto I. Potent analgesic effects of a putative sodium channel blocker M58373 on formalin-induced and neuropathic pain in rats. Eur. J. Pharmacol. 2006, 536:248-255.
2. Attal N., Bouhassira D. Can pain be more or less neuropathic?. Pain 2004, 110:510-511.
3. Attal N., Jazat F., Kayser V., Guilbaud G. Further evidence for 'pain-related' behaviours in a model of unilateral peripheral mononeuropathy. Pain 1990, 41:235-251.
4. Attal N., Rouaud J., Brasseur L., Chauvin M., Bouhassira D. Systemic lidocaine in pain due to peripheral nerve injury and predictors of response. Neurology 2004, 62:218-225.
5. Backonja M.M., Stacey B. Neuropathic pain symptoms relative to overall pain rating. J. Pain 2004, 5:491-497.
6. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
7. Blackburn-Munro G., Fleetwood-Walker S.M. The effects of Na+ channel blockers on somatosensory processing by rat dorsal horn neurones. Neuroreport 1997, 8:1549-1554.
8. Choi Y., Yoon Y.W., Na H.S., Kim S.H., Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 1994, 59:369-376.
9. Decosterd I., Woolf C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 2000, 87:149-158.
10. Djouhri L., Koutsikou S., Fang X., McMullan S., Lawson S.N. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J. Neurosci. 2006, 26:1281-1292.
11. Dowdall T., Robinson I., Meert T.F. Comparison of five different rat models of peripheral nerve injury. Pharmacol. Biochem. Behav. 2005, 80:93-108.
12. Dworkin R.H., O'Connor A.B., Backonja M., Farrar J.T., Finnerup N.B., Jensen T.S., Kalso E.A., Loeser J.D., Miaskowski C., Nurmikko T.J., Portenoy R.K., Rice A.S., Stacey B.R., Treede R.D., Turk D.C., Wallace M.S. Pharmacologic management of neuropathic pain: evidence-based recommendations. Pain 2007, 132:237-251.
13. Erichsen H.K., Blackburn-Munro G. Pharmacological characterisation of the spared nerve injury model of neuropathic pain. Pain 2002, 98:151-161.
14. Erichsen H.K., Hao J.X., Xu X.J., Blackburn-Munro G. A comparison of the antinociceptive effects of voltage-activated Na+ channel blockers in two rat models of neuropathic pain. Eur. J. Pharmacol. 2003, 458:275-282.
15. Fleetwood-Walker S.M., Quinn J.P., Wallace C., Blackburn-Munro G., Kelly B.G., Fiskerstrand C.E., Nash A.A., Dalziel R.G. Behavioural changes in the rat following infection with varicella-zoster virus. J. Gen. Virol. 1999, 80(Pt 9):2433-2436.
16. Giuliano F., Warner T.D. Ex vivo assay to determine the cyclooxygenase selectivity of non-steroidal anti-inflammatory drugs. Br. J. Pharmacol. 1999, 126:1824-1830.
17. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
18. Huntjens D.R., Spalding D.J., Danhof M., Della Pasqua O.E. Differences in the sensitivity of behavioural measures of pain to the selectivity of cyclo-oxygenase inhibitors. Eur. J. Pain 2009, 13:448-457.
19. Iadarola M.J., Brady L.S., Draisci G., Dubner R. Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioral parameters and opioid receptor binding. Pain 1988, 35:313-326.
20. Iadarola M.J., Douglass J., Civelli O., Naranjo J.R. Differential activation of spinal cord dynorphin and enkephalin neurons during hyperalgesia: evidence using cDNA hybridization. Brain Res. 1988, 455:205-212.
21. Ivanavicius S.P., Ball A.D., Heapy C.G., Westwood F.R., Murray F., Read S.J. Structural pathology in a rodent model of osteoarthritis is associated with neuropathic pain: increased expression of ATF-3 and pharmacological characterisation. Pain 2007, 128:272-282.
22. Jarvis B., Coukell A.J. Mexiletine. A review of its therapeutic use in painful diabetic neuropathy. Drugs 1998, 56:691-707.
23. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363.
24. Kingery W.S. A critical review of controlled clinical trials for peripheral neuropathic pain and complex regional pain syndromes. Pain 1997, 73:123-139.
25. Laird J.M., Carter A.J., Grauert M., Cervero F. Analgesic activity of a novel use-dependent sodium channel blocker, crobenetine, in mono-arthritic rats. Br. J. Pharmacol. 2001, 134:1742-1748.
26. Lee D.H., Iyengar S., Lodge D. The role of uninjured nerve in spinal nerve ligated rats points to an improved animal model of neuropathic pain. Eur. J. Pain 2003, 7:473-479.
27. Leith J.L., Wilson A.W., Donaldson L.F., Lumb B.M. Cyclooxygenase-1-derived prostaglandins in the periaqueductal gray differentially control C- versus A-fiber-evoked spinal nociception. J. Neurosci. 2007, 27:11296-11305.
28. Malcangio M., Tomlinson D.R. A pharmacologic analysis of mechanical hyperalgesia in streptozotocin/diabetic rats. Pain 1998, 76:151-157.
29. Marais E., Klugbauer N., Hofmann F. Calcium channel alpha(2)delta subunits-structure and Gabapentin binding. Mol. Pharmacol. 2001, 59:1243-1248.
30. Meller S.T., Cummings C.P., Traub R.J., Gebhart G.F. The role of nitric oxide in the development and maintenance of the hyperalgesia produced by intraplantar injection of carrageenan in the rat. Neuroscience 1994, 60:367-374.
31. Nagakura Y., Okada M., Kohara A., Kiso T., Toya T., Iwai A., Wanibuchi F., Yamaguchi T. Allodynia and hyperalgesia in adjuvant-induced arthritic rats: time course of progression and efficacy of analgesics. J. Pharmacol. Exp. Ther. 2003, 306:490-497.
32. Nakazato-Imasato E., Kurebayashi Y. Pharmacological characteristics of the hind paw weight bearing difference induced by chronic constriction injury of the sciatic nerve in rats. Life Sci. 2009, 84:622-626.
33. Nakazato-Imasato E., Tanimoto-Mori S., Kurebayashi Y. Effect of mexiletine on dynamic allodynia induced by chronic constriction injury of the sciatic nerve in rats. J. Vet. Med. Sci. 2009, 71:991-994.
34. Palm F., Mossner R., Chen Y., He L., Gerlach M., Bischofs S., Riederer P., Lesch K.P., Sommer C. Reduced thermal hyperalgesia and enhanced peripheral nerve injury after hind paw inflammation in mice lacking the serotonin-transporter. Eur. J. Pain 2008, 12:790-797.
35. Pedersen L.H., Blackburn-Munro G. Pharmacological characterisation of place escape/avoidance behaviour in the rat chronic constriction injury model of neuropathic pain. Psychopharmacology (Berl.) 2006, 185:208-217.
36. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., Woolf C.J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br. J. Pharmacol. 1995, 115:1265-1275.
37. Said G., Hontebeyrie-Joskowicz M. Nerve lesions induced by macrophage activation. Res. Immunol. 1992, 143:589-599.
38. Schafers M., Lee D.H., Brors D., Yaksh T.L., Sorkin L.S. Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J. Neurosci. 2003, 23:3028-3038.
39. Segond von Banchet G., Boettger M.K., Fischer N., Gajda M., Brauer R., Schaible H.G. Experimental arthritis causes tumor necrosis factor-alpha-dependent infiltration of macrophages into rat dorsal root ganglia which correlates with pain-related behavior. Pain 2009, 145:151-159.
40. Seltzer Z., Dubner R., Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990, 43:205-218.
41. Shamash S., Reichert F., Rotshenker S. The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J. Neurosci. 2002, 22:3052-3060.
42. Stanfa L.C., Singh L., Williams R.G., Dickenson A.H. Gabapentin, ineffective in normal rats, markedly reduces C-fibre evoked responses after inflammation. Neuroreport 1997, 8:587-590.
43. Taurog J.D., Argentieri D.C., McReynolds R.A. Adjuvant arthritis. Methods Enzymol. 1988, 162:339-355.
44. Tsujino H., Kondo E., Fukuoka T., Dai Y., Tokunaga A., Miki K., Yonenobu K., Ochi T., Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 2000, 15:170-182.
45. Urban M.O., Ren K., Park K.T., Campbell B., Anker N., Stearns B., Aiyar J., Belley M., Cohen C., Bristow L. Comparison of the antinociceptive profiles of gabapentin and 3-methylgabapentin in rat models of acute and persistent pain: implications for mechanism of action. J. Pharmacol. Exp. Ther. 2005, 313:1209-1216.
46. Wallace M.S., Magnuson S., Ridgeway B. Efficacy of oral mexiletine for neuropathic pain with allodynia: a double-blind, placebo-controlled, crossover study. Reg. Anesth. Pain Med. 2000, 25:459-467.
47. Wallace V.C., Segerdahl A.R., Lambert D.M., Vandevoorde S., Blackbeard J., Pheby T., Hasnie F., Rice A.S. The effect of the palmitoylethanolamide analogue, palmitoylallylamide (L-29) on pain behaviour in rodent models of neuropathy. Br. J. Pharmacol. 2007, 151:1117-1128.
48. Weiser T. Comparison of the effects of four Na+ channel analgesics on TTX-resistant Na+ currents in rat sensory neurons and recombinant Nav1.2 channels. Neurosci. Lett. 2006, 395:179-184.
49. Woolf C.J., Allchorne A., Safieh-Garabedian B., Poole S. Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br. J. Pharmacol. 1997, 121:417-424.
50. Woolf C.J., Ma Q. Nociceptors-noxious stimulus detectors. Neuron 2007, 55:353-364.