Norepinephrine-induced nociception and vasoconstrictor hypersensitivity in rats with chronic post-ischemia pain

Pain

Volumn 137, Issue 3, 2008, Pages 640-651

  Xanthos, Dimitris N ^a   Bennett, Gary J ^a   Coderre, Terence J ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Arg8 vasopressin; Adrenergic receptors; Chronic post ischemia pain; Complex regional pain syndrome; CRPS I; Ischemia; l NIO; Laser Doppler; SIN 1; Sodium nitroprusside; Vasoconstriction

Indexed keywords

LINSIDOMINE; N5 (1 IMINOETHYL)ORNITHINE; NITROPRUSSIDE SODIUM; NORADRENALIN; PRAZOSIN; VASOPRESSIN; YOHIMBINE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW; CHRONIC PAIN; CONTROLLED STUDY; DRUG HYPERSENSITIVITY; ISCHEMIA; LASER DOPPLER FLOWMETRY; MALE; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; VASOCONSTRICTION; VASODILATATION;

ANIMALS; DISEASE MODELS, ANIMAL; HINDLIMB; HYPERALGESIA; ISCHEMIA; MALE; NOREPINEPHRINE; PAIN MEASUREMENT; RATS; RATS, LONG-EVANS; REFLEX SYMPATHETIC DYSTROPHY; VASOCONSTRICTION;

EID: 47049122048     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2007.10.031     Document Type: Article

References (69)

1. Ackerman W.E., Munir M.A., and Zhang J.-M. Assessment of laser Doppler imaging for the diagnosis of complex regional pain syndrome I. J Neuro Pain Symp Pal 1 (2005) 13-20
2. Ali Z., Raja S.N., Wesselmann U., Fuchs P.N., Meyer R.A., and Campbell J.N. Intradermal injection of norepinephrine evokes pain in patients with sympathetically maintained pain. Pain 88 (2000) 161-168
3. Arnold J.M., Teasell R.W., MacLeod A.P., Brown J.E., and Carruthers S.G. Increased venous alpha-adrenoceptor responsiveness in patients with reflex sympathetic dystrophy. Ann Intern Med 118 (1993) 619-621
4. Arnér S. Intravenous phentolamine test: diagnostic and prognostic use in reflex sympathetic dystrophy. Pain 46 (1991) 17-22
5. Baron R., Schattschneider J., Binder A., Siebrecht D., and Wasner G. Relation between sympathetic vasoconstrictor activity and pain and hyperalgesia in complex regional pain syndromes: a case-control study. Lancet 359 (2002) 1655-1660
6. Berkowitz B.A., and Sherman S. Characterization of vasopressin analgesia. J Pharmacol Exp Ther 220 (1982) 329-334
7. Birder L.A., and Perl E.R. Expression of alpha2-adrenergic receptors in rat primary afferent neurones after peripheral nerve injury or inflammation. J Physiol 515 (1999) 533-542
8. Birklein F., Riedl B., Claus D., Neundörfer B., and Handwerker H.O. Cutaneous norepinephrine application in complex regional pain syndrome. Eur J Pain 1 (1997) 123-132
9. Birklein F., Riedl B., Neundörfer B., and Handwerker H.O. Sympathetic vasoconstrictor reflex pattern in patients with complex regional pain syndrome. Pain 75 (1998) 93-100
10. Campbell J.N., Raja S.N., and Meyer R.A. Painful sequelae of nerve injury. In: Dubner R., Gebhart G.F., and Bond M.R. (Eds). Proceedings of the Vth World Congress on pain (1988), Elsevier, Amsterdam 135-143
11. 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
12. Chen Y., Michaelis M., Jänig W., and Devor M. Adrenoreceptor subtype mediating sympathetic-sensory coupling in injured sensory neurons. J Neurophysiol 76 (1996) 3721-3730
13. Cho H.J., Kim D.S., Lee N.H., Kim J.K., Lee K.M., Han K.S., et al. Changes in the alpha2-adrenergic receptor subtypes gene expression in rat dorsal root ganglion in an animal model of neuropathic pain. Neuroreport 8 (1997) 3119-3122
14. Chung K., Lee B.H., Yoon Y.W., and Chung J.M. Sympathetic sprouting in the dorsal root ganglia of the injured peripheral nerve in a rat neuropathic pain model. J Comp Neurol 376 (1996) 55-63
15. Coderre T.J., Xanthos D.N., Francis L., and Bennett G.J. Chronic post-ischemia pain (CPIP): a novel animal model of complex regional pain syndrome-type I (CRPS-I; reflex sympathetic dystrophy) produced by prolonged hind paw ischemia and reperfusion in the rat. Pain 112 (2004) 94-105
16. Da S Rocha J.C., Peixoto M.E., Jancar S., Cunha F.Q., Ribeiro R.A., and da Rocha F.A. Dual effect of nitric oxide in articular inflammatory pain in zymosan-induced arthritis in rats. Br J Pharmacol 136 (2002) 588-596
17. Davis K.D., Treede R.D., Raja S.N., Meyer R.A., and Campbell J.N. Topical application of clonidine relieves hyperalgesia in patients with sympathetically maintained pain. Pain 47 (1991) 309-317
18. Devor M., and Jänig W. Activation of myelinated afferents ending in a neuroma by stimulation of the sympathetic supply in the rat. Neurosci Lett 24 (1981) 43-47
19. Devor M., Jänig W., and Michaelis M. Modulation of activity in dorsal root ganglion neurons by sympathetic activation in nerve-injured rats. J Neurophysiol 71 (1994) 38-47
20. Doursout M.F., Liang Y., and Chelly J.E. NOS inhibitors exhibit antinociceptive properties in the rat formalin test. Can J Anaesth 50 (2003) 909-916
21. Drummond P.D. The effect of noradrenaline, angiotensin II and vasopressin on blood flow and sensitivity to heat in capsaicin-treated skin. Clin Auton Res 8 (1998) 87-93
22. Drummond P.D. Nitroprusside inhibits thermal hyperalgesia induced by noradrenaline in capsaicin-treated skin. Pain 80 (1999) 405-412
23. Drummond P.D., Skipworth S., and Finch P.M. Alpha 1-adrenoceptors in normal and hyperalgesic human skin. Clin Sci 91 (1996) 73-77
24. Drummond P.D., Finch P.M., Skipworth S., and Blockey P. Pain increases during sympathetic arousal in patients with complex regional pain syndrome. Neurology 57 (2001) 1296-1303
25. Ghostine S.Y., Comair Y.G., Turner D.M., Kassell N.F., and Azar C.G. Phenoxybenzamine in the treatment of causalgia. Report of 40 cases. J Neurosurg 60 (1984) 1263-1268
26. Häbler H.-J., Eschenfelder S., Liu X.-G., and Jänig W. Sympathetic-sensory coupling after L5 spinal nerve lesion in the rat and its relation to changes in dorsal root ganglion blood flow. Pain 87 (2000) 335-345
27. Hyland W.T. Treating reflex sympathetic dystrophy with transdermal nitroglycerin. Plast Reconstr Surg 83 (1989) 195
28. Ialenti A., Ianaro A., Moncada S., and Di Rosa M. Modulation of acute inflammation by endogenous nitric oxide. Eur J Pharmacol 211 (1992) 177-182
29. Jarajapu Y.P., Coats P., McGrath J.C., MacDonald A., and Hillier C. Increased alpha(1)- and alpha(2)-adrenoceptor-mediated contractile responses of human skeletal muscle resistance arteries in chronic limb ischemia. Cardiovasc Res 49 (2001) 218-225
30. Kurvers H.A., Jacobs M.J., Beuk R.J., Van den Wildenberg F.A., Kitslaar P.J., Slaaf D.W., and Reneman R.S. Reflex sympathetic dystrophy: evolution of microcirculatory disturbances in time. Pain 60 (1995) 333-340
31. Kurvers H.A., Tangeider G.J., De Mey J.G., Slaaf D.W., Beuk R.J., van denWildenberg F.A., et al. Skin blood flow abnormalities in rat model of neuropathic pain: result of decreases sympathetic vasoconstrictor outflow?. J Auton Nerv Syst 63 (1997) 19-29
32. Kurvers H., Daemen M., Slaaf D., Stassen F., van den Wildenberg F., Kitslaar P., et al. Partial peripheral neuropathy and denervation induced adrenoceptor supersensitivity. Functional studies in an experimental model. Acta Orthop Belg 64 (1998) 64-70
33. Laferrière A, Millecamps M, Xanthos DN, Xiao WH, Bennett GJ, Coderre TJ. Chronic post-ischemia pain (CPIP): a novel animal model suggests that ischemia-reperfusion injury, no-reflow and chronic tissue ischemia contribute to complex regional pain syndrome-type I (CRPS-I). Second International Congress on neuropathic pain, Eur J Pain 11:S61-62.
34. Lee Y.H., Wei F.C., Lee J., Su M.S., and Chang Y.C. Effect of postischemic reperfusion on microcirculation and lipid metabolism of skeletal muscle. Microsurgery 16 (1995) 522-527
35. Levy D., Tal M., Hoke A., and Zochodne D.W. Transient action of the endothelial constitutive nitric oxide synthase (ecNOS) mediates the development of thermal hypersensitivity following peripheral nerve injury. Eur J Neurosci 12 (2000) 2323-2332
36. Levy D., and Zochodne D.W. NO Pain: Potential roles of nitric oxide in neuropathic pain. Pain Practice 4 (2004) 11-18
37. Mailis-Gagnon A., and Bennett G.J. Abnormal contralateral pain responses from an intradermal injection of phenylephrine in a subset of patients with complex regional pain syndrome (CRPS). Pain 111 (2004) 378-384
38. Manahan A.P., Burkman K.A., Malesker M.A., and Benecke G.W. Clinical observation on the use of topical nitroglycerin in the management of severe shoulder-hand syndrome. Nebr Med J 78 (1993) 87-89
39. McLachlan E.M., Jänig W., Devor M., and Michaelis M. Peripheral nerve injury triggers noradrenergic sprouting within dorsal root ganglia. Nature 363 (1993) 543-546
40. Michaelis M., Devor M., and Jänig W. Sympathetic modulation of activity in rat dorsal root ganglion neurons changes over time following peripheral nerve injury. J Neurophysiol 76 (1996) 753-763
41. Moncada S., Radomski M.W., and Palmer R.M. Endothelium-derived relaxing factor. Identification as nitric oxide and role in the control of vascular tone and platelet function. Biochem Pharmacol 37 (1988) 2495-2501
42. Muizelaar J.P., Kleyer M., Hertogs I.A., and DeLange D.C. Complex regional pain syndrome (reflex sympathetic dystrophy and causalgia): management with the calcium channel blocker nifedipine and/or the alpha-sympathetic blocker phenoxybenzamine in 59 patients. Clin Neurol Neurosurg 99 (1997) 26-30
43. Naik A.K., Tandan S.K., Kumar D., and Dudhgaonkar S.P. Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats. Eur J Pharmacol 530 (2006) 59-69
44. O'Halloran K.D., and Perl E.R. Effects of partial nerve injury on the responses of C-fiber polymodal nociceptors to adrenergic agonists. Brain Res 759 (1997) 233-240
45. Osborne M.G., and Coderre T.J. Effects of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia. Br J Pharmacol 126 (1999) 1840-1846
46. Raja S.N., Treede R.D., Davis K.D., and Campbell J.N. Systemic alpha-adrenergic blockade with phentolamine: a diagnostic test for sympathetically maintained pain. Anesthesiology 74 (1991) 691-698
47. Ringkamp M., Grethel E.J., Choi Y., Meyer R.A., and Raja S.N. Mechanical hyperalgesia after spinal nerve ligation in rat is not reversed by intraplantar or systemic administration of adrenergic antagonists. Pain 79 (1999) 135-141
48. Roberts W.J. A hypothesis on the physiological basis for causalgia and related pains. Pain 24 (1986) 297-311
49. Sapienza P., Edwards J.D., Mingoli J.S., McGregor P.E., Cavallari N., and Agrawal D.K. Ischemia-induced peripheral arterial vasospasm: role of alpha 1- and alpha 2-adrenoceptors. J Surg Res 62 (1996) 192-196
50. Sato J., and Perl E.R. Adrenergic excitation of cutaneous pain receptors induced by peripheral nerve injury. Science 251 (1991) 1608-1610
51. Schürmann M., Gradl G., Andress H.J., Fürst H., and Schildberg F.W. Assessment of peripheral sympathetic nervous function for diagnosing early post-traumatic complex regional pain syndrome type I. Pain 80 (1999) 149-159
52. Schürmann M., Gradl G., Zaspel J., Kayser M., Löhr P., and Andress H.J. Peripheral sympathetic function as a predictor of complex regional pain syndrome type I (CRPS I) in patients with radial fracture. Auton Neurosci 86 (2000) 127-134
53. Seasholtz T.M., Cai G., Wang H.Y., and Friedman E. Selected contribution: effects of ischemia-reperfusion on vascular contractility and alpha(1)-adrenergic-receptor signalling in the rat tail artery. J Appl Physiol 91 (2001) 1004-1010
54. Semmes J., Weinstein S., Ghent L., and Teuber H.-L. Somatosensory changes after penetrating brain wounds in man (1960), Harvard University Press, Cambridge, MA
55. Tao F., Tao Y.X., Zhao C., Dore S., Liaw W.J., Raja S.N., et al. Differential roles of neuronal and endothelial nitric oxide synthases during carrageenan-induced inflammatory hyperalgesia. Neuroscience 128 (2004) 421-430
56. Teasell R.W., and Arnold J.M. Alpha-1 adrenoceptor hyperresponsiveness in three neuropathic pain states: complex regional pain syndrome 1; diabetic peripheral neuropathic pain and central pain states following spinal cord injury. Pain Res Manag 9 (2004) 89-97
57. Thomas G.D., and Victor R.G. Nitric oxide mediates contraction-induced attenuation of sympathetic vasoconstriction in rat skeletal muscle. J Physiol 506 (1998) 817-826
58. Thurston C.L., Campbell I.G., Culhane E.S., Carstens E., and Watkins L.R. Characterization of intrathecal vasopressin-induced antinociception, scratching behavior, and motor suppression. Peptides 13 (1992) 17-25
59. Torebjörk E., Wahren L., Wallin G., Hallin R., and Koltzenburg M. Noradrenaline-evoked pain in neuralgia. Pain 63 (1995) 11-20
60. Tracey D.J., Cunningham J.E., and Romm M.A. Peripheral hyperalgesia in experimental neuropathy: mediation by alpha 2-adrenoreceptors on post-ganglionic sympathetic terminals. Pain 60 (1995) 317-327
61. Wall P.D., and Gutnick M. Ongoing activity in peripheral nerves: the physiology and pharmacology of impulses originating from a neuroma. Exp Neurol 43 (1974) 580-593
62. Wallin G., Torebjörk E., and Hallin R. Preliminary observations on the pathophysiology of hyperalgesia in the causalgic pain syndrome. In: Zotterman Y. (Ed). Sensory functions of the skin in primates (1976), Pergamon, New York 489-502
63. Wang W.Z., Anderson G., Fleming J.T., Peter F.W., Franken R.J., Acland R.D., et al. Lack of nitric oxide contributes to vasospasm during ischemia/reperfusion injury. Plast Reconstr Surg 99 (1997) 1099-1108
64. Wasner G., Heckmann K., Maier C., and Baron R. Vascular abnormalities in acute reflex sympathetic dystrophy (CRPS I): complete inhibition of sympathetic nerve activity with recovery. Arch Neurol 56 (1999) 613-620
65. Wasner G., Schattschneider J., Heckmann K., Maier C., and Baron R. Vascular abnormalities in reflex sympathetic dystrophy (CRPS I): mechanisms and diagnostic value. Brain 124 (2001) 587-599
66. Xanthos DN, Coderre TJ. Contribution of sympathetic activity and adrenergic receptors to nociception in an animal model of complex regional pain syndrome type I (CRPS-I; RSD) induced by ischemia-reperfusion injury of the rat hind paw. Poster presentation, 2005 IASP World Congress, Sydney, Australia.
67. Xanthos DN, Coderre TJ. Sympathetic vasoconstrictor antagonism and vasodilatation relieve mechanical allodynia in rats with chronic post-ischemia pain (CPIP). J Pain; submitted.
68. Xie J., Lee Y.H., Wang C., Chung J.M., and Chung K. Differential expression alpha1-adrenoceptor subtype mRNAs in the dorsal root ganglion after spinal nerve ligation. Brain Res Mol Brain Res 93 (2001) 164-172
69. Yen L.D., Bennett G.J., and Ribeiro-da-Silva A. Sympathetic sprouting and changes in nociceptive sensory innervation in the glabrous skin of the rat hind paw following partial peripheral nerve injury. J Comp Neurol 495 (2006) 679-690