Opioid-induced hyperalgesia in a murine model of postoperative pain: Role of nitric oxide generated from the inducible nitric oxide synthase

Anesthesiology

Volumn 104, Issue 3, 2006, Pages 546-555

  Célérier, Evelyne ^a   González, Juan R ^b   Maldonado, Rafael ^c   Cabañero, David ^a   Puig, Margarita M ^d  

^a INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^b Barcelona Biomedical Research Park   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d HOSPITAL DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALFENTANIL; FENTANYL; FENTANYL CITRATE; INDUCIBLE NITRIC OXIDE SYNTHASE; LIMIFEN; NITRIC OXIDE; OPIATE; REMIFENTANIL; SEVOFLURANE; NARCOTIC ANALGESIC AGENT; PIPERIDINE DERIVATIVE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; CONFERENCE PAPER; CONTROLLED STUDY; DRUG EFFICACY; FOOT SURGERY; GENE DELETION; HYPERALGESIA; INTRAOPERATIVE PERIOD; KNOCKOUT MOUSE; MOUSE; NOCICEPTION; NONHUMAN; POSTOPERATIVE PAIN; PRIORITY JOURNAL; SKIN INCISION; ANIMAL; ARTICLE; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; GENETICS; MALE; PHYSIOLOGY; SPECIES DIFFERENCE;

ANALGESICS, OPIOID; ANIMALS; FENTANYL; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PAIN, POSTOPERATIVE; PIPERIDINES; SPECIES SPECIFICITY;

EID: 33645523617     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/00000542-200603000-00023     Document Type: Conference Paper

References (65)

1. Mao J: Opioid-induced abnormal pain sensitivity: Implications in clinical opioid therapy. Pain 2002; 100:213-7
2. Simonnet G, Rivat C: Opioid-induced hyperalgesia: Abnormal or normal pain?. NeuroReport 2003; 14:1-6
3. Eisenach JC: Preemptive hyperalgesia, not analgesia? ANESTHESIOLOGY 2000; 92:308-9
4. Guignard B, Bossard AE, Coste C, Sessler DI, Lebrauld C, Alfonsi P, Fletcher D Chavin M,: Acute opioid tolerance: Intraoperative remifentanil increases postoperative pain and morphine requirement. ANESTHESIOLOGY 2000; 93:409-17
5. Laulin JP, Maurette P, Corcuff JB, Rivat C, Chauvin M, Simonnet G: The role of ketamine in preventing fentanyl-induced hyperalgesia and subsequent acute morphine tolerance. Anesth Analg 2002; 94:1263-9
6. Luginbuhl M, Gerber A, Schnider TW, Petersen-Felix S, Arendt-Nielsen L, Curatolo M: Modulation of remifentanil-induced analgesia, hyperalgesia, and tolerance by small-dose ketamine in humans. Anesth Analg 2003; 96:726-32
7. Derroche N, Lebrun F, Levron JC, Chauvin M, Debaene B: Influence of perioperative opioid on postoperative pain after major abdominal surgery: Sufentanil TCI versus remifentanil TCI. A randomized, controlled study. Br J Anaesth 2003; 91:842-9
8. Koppert W, Sittl R, Scheuber K, Alsheimer M, Schmelz M, Schuttler J: Differential modulation of remifentanil-induced analgesia and post-infusion hyperalgesia by S-ketamine and clonidine in humans. ANESTHESIOLOGY 2003; 99:152-9
9. Richebé P, Rivat C, Laulin JP, Maurette P, Simonnet G: Ketamine improves the management of exaggerated postoperative pain observed in perioperative fentanyl-treated rats. ANESTHESIOLOGY 2005; 102:421-8
10. Kissin I, Brown PT, Bradley EL: Magnitude of acute tolerance to opioid is not related to their potency. ANESTHESIOLOGY 1991; 75:913-6
11. Kissin I, Lee SS, Arthur GR, Bradley EL: Time course characteristics of acute tolerance development to continuously infused alfentanil in rats. Anesth Analg 1996; 83:600-5
12. Pogatzki EM, Raja SN: A mouse model of incisional pain. ANESTHESIOLOGY 2003; 99:1023-7
13. Li X, Angst MS, Clark JD: A murine model of opioid-induced hyperalgesia. Mol Brain Res 2001; 86:56-62
14. Célérier E, Simonnet G, Maldonado R: Prevention of fentanyl-induced delayed pronociceptive effects in mice lacking the protein kinase Cγ; gene. Neuropharmacology 2004; 46:264-72
15. Rivat C, Laulin JP, Corcuff JB, Celerier E, Pain L, Simonnet G: Fentanyl enhancement of carrageenan-induced long-lasting hyperalgesia in rats: prevention by the N-methyl-D-aspartate receptor antagonist ketamine. ANESTHESIOLOGY 2002; 96:381-91
16. Li X, Angst MS, Clark JD: Opioid-induced hyperalgesia and incisional pain. Anesth Analg 2001; 93:204-9
17. Célérier E, Rivat C, Jun Y, Laulin JP, Larcher A, Reynier P, Simonnet G: Long-lasting hyperalgesia induced by fentanyl in rats: Preventive effect of ketamine. ANESTHESIOLOGY 2000; 92:465-72
18. Mayers I, Johnson D: The nonspecific inflammatory response to injury. Can J Anaesthesia 1998; 45:871-9
19. Melzack R, Coderre TJ, Katz J, Vaccarino AL: Central neuroplasticity and pathological pain. Ann N Y Acad Sci 2001; 933:157-74
20. Garthwaite J, Charles SL, Chess-Williams R: Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role a intracellular messenger in the brain. Nature 1988; 336:385-8
21. Snyder SH: Nitric oxide: First in a new class of neurotransmitters. Science 1992; 41:494-6
22. Gonzalez-Hernandez T, Rustioni A: Expression of three forms of nitric oxide synthase in peripheral nerve regeneration. J Neurosci Res 1999; 55:198-207
23. Nathan C, Xie QW: Regulation of biosynthesis of nitric oxide. J Biol Chem 1994; 269:13725-8
24. Coleman JW: Nitric oxide in immunity and inflammation. Int Immunopharmacol 2001; 1:1397-406
25. Guhring H, Gorig M, Ates M, Coste O, Zeilhofer HU, Pahl A, Rehse K, Brune K: Suppressed injury-induced rise in spinal prostaglandin E2 production and reduced early thermal hyperalgesia in iNOS-deficient mice. J Neurosci 2000; 20:6714-20
26. Tao F, Tao YX, Mao P, Zhao C, Li D, Liaw WJ, Raja SN, Johns RA: Intact carrageenan-induced thermal hyperalgesia in mice lacking inducible nitric oxide synthase. Neuroscience 2003; 120:847-54
27. Sung CS, Wen ZH, Chang WK, Ho ST, Tsai SK, Chang YC, Wong CS: Intrathecal interleukin-1β administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord. Brain Res 2004; 1015:145-53
28. Wu WP, Hao JX, Ongini E, Impagnatiello F, Presotto C, Wiesenfeld-Hallin Z, Xu XJ: A nitric oxide (NO)-releasing derivative of gabapentin, NCX 8001, alleviates neuropathic pain-like behavior after spinal cord and peripheral nerve injury. Br J Pharmacol 2004; 141:65-74
29. Wong CS, Hsu MM, Chou YY, Tao PL, Tung CS: Morphine tolerance increases [3H]MK-801 binding affinity and constitutive neuronal nitric oxide synthase expression in rat spinal cord. Br J Anaesth 2000; 85:587-91
30. Powell KJ, Hosokawa A, Bell A, Sutak M, Milne B, Quirion R, Jhamandas K: Comparative effects of cyclo-oxygenase and nitric oxide synthase inhibition on the development and reversal of spinal opioid tolerance. Br J Pharmacol 1999; 127:631-44
31. Li X, Clark JD: Spinal cord nitric oxide synthase and heme oxygenase limit morphine induced analgesia. Mol Brain Res 2001; 95:96-102
32. Ozek M, Uresin Y, Gungor M: Comparison of the effects of specific and nonspecific inhibition of nitric oxide synthase on morphine analgesia, tolerance and dependence in mice. Life Sci 2003; 72:1943-51
33. Guide for Care and Use of Laboratory Animals. Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council. Washington, DC, National Academy Press, 1996
34. Lozito RJ, La Marca S, Dunn RW, Jerussi TP: Single versus multiple infusions of fentanyl analogues in a rat EEG model. Life Sci 1994; 55:1337-42
35. Cox EH, Kuipers JA, Danhof M: Pharmacokinetic-pharmacodynamic modeling of the EEG effect of alfentanil in rats: assessment of rapid functional adaptation. Br J Pharmacol 1998; 124:1534-40
36. Criado AB, Gomez E Segura IA: Reduction of isoflurane MAC by fentanyl or remifentanil in rats. Vet Anaesth Analg 2003; 30:250-6
37. Brennan TJ, Vandermeulen EP, Gebhart GF: Characterization of a rat model of incisional pain. Pain 1996; 64:493-501
38. 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
39. Randall LO, Selitto JJ: A method for measurement of analgesic activity on inflamed tissue. Arch Int Pharmacodynam 1957; 111:409-19
40. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL: Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Meth 1994; 53:55-63
41. Pinheiro JC, Bates DM: Mixed-effects models, S and S-PLUS, Statistics and Computing Series. New York, Springer-Verlag, 2000, pp 1-528
42. Liu S, Carpenter R, Mackey DC, Thirlby RC, Rupp SM, Shine TS, Feinglass NG, Metzger PP, Fulmer JT, Smith SL: Effects of preoperative analgesic technique on rate of recovery after colon surgery. ANESTHESIOLOGY 1995; 83:757-65
43. Minkowitz H: Postoperative pain management in patients undergoing major surgery after remifentanil versus fentanyl anesthesia. Multicentre Investigator Group. Can J Anaesth 2000; 47:522-8
44. Dershwitz M, Randel GI, Rosow CE, Fragen RJ, Conners PM, Librojo ES, Shaw DL, Peng AW, Jamerson BD: Initial clinical experience with remifentanil, a new opioid metabolized by esterases. Anesth Analg 1995; 81:619-23
45. Yarmush J, D'Angelo R, Kikhart B, O'Leary C, Pitts MC, Graf G, Sebel P, Watkins WD, Miguel R, Streisand J, Maysick LK, Vujic D: A comparison of remifentanil and morphine sulfate for acute postoperative analgesia after total intravenous anesthesia with remifentanil and propofol. ANESTHESIOLOGY 1997; 97:235-43
46. Fletcher D, Pinaud M, Scherpereel P, Clyti N, Chauvin M: Efficacy of 0.15 mg/kg versus 0.25 mg/kg intraoperative morphine for immediate postoperative analgesia after remifentanil-based anesthesia for major surgery. Anesth Analg 2000; 90:666-71
47. Thompson JP, Rowbotham DJ: Remifentanil: An opioid for the 21st century. Br J Anaesth 1996; 76:341-3
48. Guntz E, Dumont H, Rousel C, Gall D, Dufrasne F, Cuvelier L, Blum D, Schiffmann SN, Sosnowski M: Effects of remifentanil on N-methyl-D-aspartate receptor: An electrophysiological study in rat spinal cord. ANESTHESIOLOGY 2005; 102:1235-41
49. Whiteside GT, Harrison J, Boulet J, Mark L, Pearson M, Gottshall S, Walker K: Pharmacological characterization of a rat model of incisional pain. Br J Pharmacol 2004; 141:85-91
50. Laulin JP, Célérier E, Larcher A, Le Moal M, Simonnet G: Opiate tolerance to daily heroin administration: An apparent phenomenon associated with enhanced pain sensitivity. Neuroscience 1999; 89:631-6
51. Célérier E, Laulin J, Larcher A, Le Moal M, Simonnet G: Evidence for opiate-activated NMDA processes masking opiate analgesia in rats. Brain Res 1999; 847:18-25
52. Vinik HR, Igor K: Rapid development of tolerance to analgesia during remifentanil infusion in humans. Anesth Analg 1998; 86:1307-11
53. Osbone MG, Coderre TJ: Effects of intrathecal administration of nitric oxide synthase inhibitors on carrageenan-induced thermal hyperalgesia. Br J Pharmacol 1999; 126:1840-6
54. Mashimo H, Goyal RJ: Lessons from genetically engineered animal models: IV. Nitric oxide synthase gene knockout mice. Am J Physiol Gastrointest Liver Physiol 1999; 277:G745-50
55. Meller ST, Dykstra C, Grzybycki D, Murphy S, Gebhart GF: The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology 1994; 33:1471-8
56. Lee SC, Brosnan CF: Cytokine regulation of iNOS expression in human glial cells. Methods 1996; 10:31-7
57. Barker JE, Strangward HM, Brand MP, Hurst RD, Land JM, Clark JB, Heales SJ: Increased inducible nitric oxide synthase protein but limited nitric oxide formation occurs in astrocytes of the hph-1 (tetrahydrobiopterin deficient) mouse. Brain Res 1998; 804:1-6
58. Maihöfner C, Euchenhofer C, Tegeder I, Beck KF, Pfeilschifter J, Geisslinger G: Regulation and immunohistochemical localization of nitric oxide synthase and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation. Neurosci Lett 2000; 290:71-5
59. Wu J, Lin Q, Lu Y, Willis WD, Westlund KN: Changes in nitric oxide synthase isoforms in the spinal cord of rat following induction of chronic arthritis. Exp Brain Res 1998; 118:457-65
60. Zahn PK, Brennan TJ: Lack of effect of intrathecally administered N-methyl-D-aspartate receptor antagonists in a rat model for postoperative pain. ANESTHESIOLOGY 1998; 88:143-56
61. Omote K, Hazama K, Kawamata T, Kawamata M, Nakayaka Y, Toriyabe M, Namiki A: Peripheral nitric oxide in carrageenan-induced inflammation. Brain Res 2001; 912:171-5
62. Witte MB, Barbul A: Role of nitric oxide in wound repair. Am J Surg 2002; 183:406-12
63. Rivot JP, Sousa A, Montagne-Clavel J, Besson JM: Nitric oxide (NO) release by glutamate and NMDA in the dorsal horn of the spinal cord and in vivo electrochemical approach in the rat. Brain Res 1999; 821:101-10
64. Tao YX, Johns RA: Activation of cGMP-dependent protein kinase Ialpha is required for N-methyl-D-aspartate or nitric oxide-produced spinal thermal hyperalgesia. Eur J Pharmacol 2000; 392:141-5
65. Tao YX, Johns RA: Activation and up-regulation of spinal cord nitric oxide receptor, soluble guanylate cyclase, after formalin injection into the rat hind paw. Neuroscience 2002; 112:439-46