Spinally applied ketamine or morphine attenuate peripheral inflammation and hyperalgesia in acute and chronic phases of experimental arthritis

Brain, Behavior, and Immunity

Volumn 24, Issue 3, 2010, Pages 474-485

  Boettger, Michael Karl ^a   Weber, Konstanze ^a   Gajda, Mieczyslaw ^a   Bräuer, Rolf ^a   Schaible, Hans Georg ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Dorsal root reflex; Inflammation; Intrathecal; Ketamine; Morphine

Indexed keywords

KETAMINE; MORPHINE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN INDUCED ARTHRITIS; ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; ARTHRITIS; ARTICLE; CONTROLLED STUDY; DISEASE CLASSIFICATION; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG EFFICACY; FEMALE; HISTOPATHOLOGY; HYPERALGESIA; INFLAMMATION; JOINT SWELLING; LOCOMOTION; MAINTENANCE THERAPY; NONHUMAN; PRIORITY JOURNAL; RAT; RISK REDUCTION; SPINAL CORD;

ANALGESICS, OPIOID; ANESTHETICS, DISSOCIATIVE; ANIMALS; ARTHRITIS, EXPERIMENTAL; CHRONIC DISEASE; FEMALE; HYPERALGESIA; INFUSION PUMPS, IMPLANTABLE; INJECTIONS, SPINAL; KETAMINE; LAMENESS, ANIMAL; LAMINECTOMY; LOCOMOTION; MORPHINE; PAIN MEASUREMENT; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, INBRED LEW; SPINAL CORD;

EID: 77951621024     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.12.002     Document Type: Article

References (70)

1. Ahuja B.R. Analgesic effect of intrathecal ketamine in rats. Br. J. Anaesth. 1983, 55:991-995.
2. Annetta M.G., Iemma D., Garisto C., Tafani C., Proietti R. Ketamine: new indications for an old drug. Curr. Drug Targets 2005, 6:789-794.
3. Bär K.J., Natura G., Telleria-Diaz A., Teschner P., Vogel R., Vasquez E., Schaible H.G., Ebersberger A. Changes in the effect of spinal prostaglandin E2 during inflammation: prostaglandin E (EP1-EP4) receptors in spinal nociceptive processing of input from the normal or inflamed knee joint. J. Neurosci. 2004, 24:642-651.
4. Bigler D., Christensen C.B., Eriksen J., Jensen N.H. Morphine, morphine-6-glucuronide and morphine-3-glucuronide concentrations in plasma and cerebrospinal fluid during long-term high-dose intrathecal morphine administration. Pain 1990, 41:15-18.
5. Boettger M.K., Hensellek S., Richter F., Gajda M., Stöckigt R., Segond von Banchet G., Bräuer R., Schaible H.G. Antinociceptive effects of tumor necrosis factor alpha neutralization in a rat model of antigen-induced arthritis: evidence of a neuronal target. Arthritis Rheum. 2008, 58:2368-2378.
6. Boettger M.K., Üceyler N., Zelenka M., Schmitt A., Reif A., Chen Y., Sommer C. Differences in inflammatory pain in nNOS-, iNOS- and eNOS-deficient mice. Eur. J. Pain 2007, 11:810-818.
7. Boettger M.K., Weber K., Schmidt M., Gajda M., Bräuer R., Schaible H.G. Gait abnormalities differentially indicate pain or structural joint damage in monoarticular antigen-induced arthritis. Pain 2009, 145:142-150.
8. Boettger, M.K., Weishaupt, A., Geis, C., Toyka, K.V., Sommer, C., 2009b. Mild experimental autoimmune encephalitis as a tool to induce blood-brain barrier dysfunction. J. Neural Transm. doi: doi:10.1007/s00702-009-0342-6.
9. Boyle D.L., Jones T.L., Hammaker D., Svensson C.I., Rosengren S., Albani S., Sorkin L., Firestein G.S. Regulation of peripheral inflammation by spinal p38 MAP kinase in rats. PLoS Med. 2006, 3:e338.
10. Boyle D.L., Moore J., Yang L., Sorkin L.S., Firestein G.S. Spinal adenosine receptor activation inhibits inflammation and joint destruction in rat adjuvant-induced arthritis. Arthritis Rheum. 2002, 46:3076-3082.
11. Brock S.C., Tonussi C.R. Intrathecally injected morphine inhibits inflammatory paw edema: the involvement of nitric oxide and cyclic-guanosine monophosphate. Anesth. Analg. 2008, 106:965-971.
12. Buerkle H., Yaksh T.L. Comparison of the spinal actions of the mu-opioid remifentanil with alfentanil and morphine in the rat. Anesthesiology 1996, 84:94-102.
13. Burton A.W., Lee D.H., Saab C., Chung J.M. Preemptive intrathecal ketamine injection produces a long-lasting decrease in neuropathic pain behaviors in a rat model. Reg. Anesth. Pain Med. 1999, 24:208-213.
14. Capellino S., Straub R.H. Neuroendocrine immune pathways in chronic arthritis. Best Pract. Res. Clin. Rheumatol. 2008, 22:285-297.
15. Cervero F., Laird J.M. Mechanisms of touch-evoked pain (allodynia): a new model. Pain 1996, 68:13-23.
16. Chao C.C., Hu S., Shark K.B., Sheng W.S., Gekker G., Peterson P.K. Activation of mu opioid receptors inhibits microglial cell chemotaxis. J. Pharmacol. Exp. Ther. 1997, 281:998-1004.
17. Daher J.B., de Melo M.D., Tonussi C.R. Evidence for a spinal serotonergic control of the peripheral inflammation in the rat. Life Sci. 2005, 76:2349-2359.
18. Daher J.B., Tonussi C.R. A spinal mechanism for the peripheral anti-inflammatory action of indomethacin. Brain Res. 2003, 962:207-212.
19. del Rey A., Wolff C., Wildmann J., Randolf A., Hahnel A., Besedovsky H.O., Straub R.H. Disrupted brain-immune system-joint communication during experimental arthritis. Arthritis Rheum. 2008, 58:3090-3099.
20. Dickenson A.H., Chapman V., Green G.M. The pharmacology of excitatory and inhibitory amino acid-mediated events in the transmission and modulation of pain in the spinal cord. Gen. Pharmacol. 1997, 28:633-638.
21. Ghorpade A., Advokat C. Evidence of a role for N-methyl-d-aspartate (NMDA) receptors in the facilitation of tail withdrawal after spinal transection. Pharmacol. Biochem. Behav. 1994, 48:175-181.
22. Goebeler M., Henseleit U., Roth J., Sorg C. Substance P and calcitonin gene-related peptide modulate leukocyte infiltration to mouse skin during allergic contact dermatitis. Arch. Dermatol. Res. 1994, 286:341-346.
23. Griffiths R.J. Characterisation and pharmacological sensitivity of antigen arthritis induced by methylated bovine serum albumin in the rat. Agents Actions 1992, 35:88-95.
24. 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.
25. Härle P., Möbius D., Carr D.J., Schölmerich J., Straub R.H. An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis. Arthritis Rheum. 2005, 52:1305-1313.
26. Hruska R.E., Kennedy S., Silbergeld E.K. Quantitative aspects of normal locomotion in rats. Life Sci. 1979, 25:171-179.
27. Joris J., Costello A., Dubner R., Hargreaves K.M. Opiates suppress carrageenan-induced edema and hyperthermia at doses that inhibit hyperalgesia. Pain 1990, 43:95-103.
28. Kawasaki T., Ogata M., Kawasaki C., Ogata J., Inoue Y., Shigematsu A. Ketamine suppresses proinflammatory cytokine production in human whole blood in vitro. Anesth. Analg. 1999, 89:665-669.
29. Kyrkanides S., Fiorentino P.M., Miller J.N., Gan Y., Lai Y.C., Shaftel S.S., Puzas J.E., Piancino M.G., O'Banion M.K., Tallents R.H. Amelioration of pain and histopathologic joint abnormalities in the Col1-IL-1beta(XAT) mouse model of arthritis by intraarticular induction of mu-opioid receptor into the temporomandibular joint. Arthritis Rheum. 2007, 56:2038-2048.
30. Laurido C., Pelissier T., Perez H., Flores F., Hernandez A. Effect of ketamine on spinal cord nociceptive transmission in normal and monoarthritic rats. Neuroreport 2001, 12:1551-1554.
31. Levine J.D., Dardick S.J., Roizen M.F., Helms C., Basbaum A.I. Contribution of sensory afferents and sympathetic efferents to joint injury in experimental arthritis. J. Neurosci. 1986, 6:3423-3429.
32. Liu H., Wang H., Sheng M., Jan L.Y., Jan Y.N., Basbaum A.I. Evidence for presynaptic N-methyl-d-aspartate autoreceptors in the spinal cord dorsal horn. Proc. Natl. Acad. Sci. USA 1994, 91:8383-8387.
33. Milligan E.D., Watkins L.R. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 2009, 10:23-36.
34. Mudge A.W., Leeman S.E., Fischbach G.D. Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration. Proc. Natl. Acad. Sci. USA 1979, 76:526-530.
35. Neugebauer V., Lucke T., Schaible H.G. N-Methyl-d-aspartate (NMDA) and non-NMDA receptor antagonists block the hyperexcitability of dorsal horn neurons during development of acute arthritis in rat's knee joint. J. Neurophysiol. 1993, 70:1365-1377.
36. Oberdisse E. Allgemeine Pharmakologie. Pharmakologie und Toxikologie 1997, 3-74. Springer, Berlin, Heidelberg, New York. E. Oberdisse, E. Hackenthal, K. Kuschinsky (Eds.).
37. Okura T., Komiyama N., Morita Y., Kimura M., Yamada S. Different effects of morphine and morphine-6beta-glucuronide on formalin-evoked spinal glutamate release in conscious and freely moving rats. Neurosci. Lett. 2007, 415:169-173.
38. Ossipov M.H., Lai J., King T., Vanderah T.W., Porreca F. Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 2005, 80:319-324.
39. Parada-Turska J., Rzeski W., Majdan M., Kandefer-Szerszen M., Turski W.A. Effect of glutamate receptor antagonists and antirheumatic drugs on proliferation of synoviocytes in vitro. Eur. J. Pharmacol. 2006, 535:95-97.
40. Pavlov V.A., Tracey K.J. The cholinergic anti-inflammatory pathway. Brain Behav. Immun. 2005, 19:493-499.
41. Price T.J., Cervero F., Gold M.S., Hammond D.L., Prescott S.A. Chloride regulation in the pain pathway. Brain Res. Rev. 2009, 60:149-170.
42. Przewlocki R., Przewlocka B. Opioids in chronic pain. Eur. J. Pharmacol. 2001, 429:79-91.
43. Ren K., Williams G.M., Hylden J.L., Ruda M.A., Dubner R. The intrathecal administration of excitatory amino acid receptor antagonists selectively attenuated carrageenan-induced behavioral hyperalgesia in rats. Eur. J. Pharmacol. 1992, 219:235-243.
44. Rice A.S., Cimino-Brown D., Eisenach J.C., Kontinen V.K., Lacroix-Fralish M.L., Machin I., Mogil J.S., Stohr T. Animal models and the prediction of efficacy in clinical trials of analgesic drugs: a critical appraisal and call for uniform reporting standards. Pain 2008, 139:243-247.
45. Sastry B.R. Morphine and met-enkephalin effects on sural Adelta afferent terminal excitability. Eur. J. Pharmacol. 1978, 50:269-273.
46. Schaible H.G., Richter F., Ebersberger A., Boettger M.K., Vanegas H., Natura G., Vazquez E., Segond von Banchet G. Joint pain. Exp. Brain Res. 2009, 196:153-162.
47. Scott J.R., Tamura R.N., Muangman P., Isik F.F., Xie C., Gibran N.S. Topical substance P increases inflammatory cell density in genetically diabetic murine wounds. Wound Repair Regen. 2008, 16:529-533.
48. Segond von Banchet G., Boettger M.K., Fischer N., Gajda M., Bräuer 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.
49. Shenker N., Haigh R., Roberts E., Mapp P., Harris N., Blake D. A review of contralateral responses to a unilateral inflammatory lesion. Rheumatology (Oxford) 2003, 42:1279-1286.
50. Shibakawa Y.S., Sasaki Y., Goshima Y., Echigo N., Kamiya Y., Kurahashi K., Yamada Y., Andoh T. Effects of ketamine and propofol on inflammatory responses of primary glial cell cultures stimulated with lipopolysaccharide. Br. J. Anaesth. 2005, 95:803-810.
51. Shimaoka M., Iida T., Ohara A., Taenaka N., Mashimo T., Honda T., Yoshiya I. Ketamine inhibits nitric oxide production in mouse-activated macrophage-like cells. Br. J. Anaesth. 1996, 77:238-242.
52. Sluka K.A., Jordan H.H., Willis W.D., Westlund K.N. Differential effects of N-methyl-d-aspartate (NMDA) and non-NMDA receptor antagonists on spinal release of amino acids after development of acute arthritis in rats. Brain Res. 1994, 664:77-84.
53. Sluka K.A., Lawand N.B., Westlund K.N. Joint inflammation is reduced by dorsal rhizotomy and not by sympathectomy or spinal cord transection. Ann. Rheum. Dis. 1994, 53:309-314.
54. Sluka K.A., Westlund K.N. Centrally administered non-NMDA but not NMDA receptor antagonists block peripheral knee joint inflammation. Pain 1993, 55:217-225.
55. Sluka K.A., Willis W.D., Westlund K.N. Joint inflammation and hyperalgesia are reduced by spinal bicuculline. Neuroreport 1993, 5:109-112.
56. Sorkin L.S., Moore J., Boyle D.L., Yang L., Firestein G.S. Regulation of peripheral inflammation by spinal adenosine: role of somatic afferent fibers. Exp. Neurol. 2003, 184:162-168.
57. Sorkin L.S., Westlund K.N., Sluka K.A., Dougherty P.M., Willis W.D. Neural changes in acute arthritis in monkeys. IV. Time-course of amino acid release into the lumbar dorsal horn. Brain Res. Brain Res. Rev. 1992, 17:39-50.
58. Straub R.H., Grum F., Strauch U., Capellino S., Bataille F., Bleich A., Falk W., Scholmerich J., Obermeier F. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut 2008, 57:911-921.
59. Turnbull A.V., Rivier C.L. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol. Rev. 1999, 79:1-71.
60. Vasquez E., Bär K.J., Ebersberger A., Klein B., Vanegas H., Schaible H.G. Spinal prostaglandins are involved in the development but not the maintenance of inflammation-induced spinal hyperexcitability. J. Neurosci. 2001, 21:9001-9008.
61. Villetti G., Bergamaschi M., Bassani F., Bolzoni P.T., Maiorino M., Pietra C., Rondelli I., Chamiot-Clerc P., Simonato M., Barbieri M. Antinociceptive activity of the N-methyl-d-aspartate receptor antagonist N-(2-Indanyl)-glycinamide hydrochloride (CHF3381) in experimental models of inflammatory and neuropathic pain. J. Pharmacol. Exp. Ther. 2003, 306:804-814.
62. Waldburger J.M., Boyle D.L., Edgar M., Sorkin L.S., Levine Y.A., Pavlov V.A., Tracey K., Firestein G.S. Spinal p38 MAP kinase regulates peripheral cholinergic outflow. Arthritis Rheum. 2008, 58:2919-2921.
63. Walker J.S., Chandler A.K., Wilson J.L., Binder W., Day R.O. Effect of mu-opioids morphine and buprenorphine on the development of adjuvant arthritis in rats. Inflamm. Res. 1996, 45:557-563.
64. Wang Y., Huang C., Cao Y., Han J.S. Repeated administration of low dose ketamine for the treatment of monoarthritic pain in the rat. Life Sci. 2000, 67:261-267.
65. Watkins L.R., Hutchinson M.R., Milligan E.D., Maier S.F. " Listening" and " talking" to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Brain Res. Rev. 2007, 56:148-169.
66. Whiteside G.T., Harrison J., Boulet J., Mark L., Pearson M., Gottshall S., Walker K. Pharmacological characterisation of a rat model of incisional pain. Br. J. Pharmacol. 2004, 141:85-91.
67. Willis W.D. Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp. Brain Res. 1999, 124:395-421.
68. Yaksh T.L., Kohl R.L., Rudy T.A. Induction of tolerance and withdrawal in rats receiving morphine in the spinal subarachnoid space. Eur. J. Pharmacol. 1977, 42:275-284.
69. Yaksh T.L., Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 1976, 17:1031-1036.
70. Zhang Y., Conklin D.R., Li X., Eisenach J.C. Intrathecal morphine reduces allodynia after peripheral nerve injury in rats via activation of a spinal A1 adenosine receptor. Anesthesiology 2005, 102:416-420.