Non-nociceptive environmental stress induces hyperalgesia, not analgesia, in pain and opioid-experienced rats

Neuropsychopharmacology

Volumn 32, Issue 10, 2007, Pages 2217-2228

  Rivat, Cyril ^a   Laboureyras, Emilie ^a   Laulin, Jean Paul ^a   Le Roy, Chloé ^a   Richebé, Philippe ^a,b   Simonnet, Guy ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

Analgesia; Hyperalgesia; Opioid; Pain sensitization; Stress

Indexed keywords

BN 2572; FENTANYL CITRATE; GACYCLIDINE; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NALTREXONE; OPIATE; UNCLASSIFIED DRUG;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENVIRONMENTAL STRESS; HYPERALGESIA; LOW DRUG DOSE; MALE; NOCICEPTION; NONHUMAN; PAIN; PAIN THRESHOLD; PATHOGENESIS; PRIORITY JOURNAL; RAT; SENSITIZATION;

EID: 34548699166     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301340     Document Type: Article

References (47)

1. Akil H, Madden JH, Patrick RL, Barchas JD (1976). Stress-induced increase in endogenous opiate peptides: concurrent analgesia and its partial reversal by naloxone. In: Kosterlitz HW (ed). Opiates and Endogenous Opioid Peptides. North-Holland: Amsterdam. pp 63-70.
2. Angst MS, Clark JD (2006). Opioid-induced hyperalgesia: a qualitative systematic review. Anesthesiology 104: 570-587.
3. Angst MS, Koppert W, Pahl I, Clark DJ, Schmelz M (2003). Short-term infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 106: 49-57.
4. Bespalov AY, Zvartau EE, Beardsley PM (2001). Opioid-NMDA receptor interactions may clarify conditioned (associative) components of opioid analgesic tolerance. Neurosci Biobehav Rev 25: 343-353.
5. Bradesi S, Schwetz I, Ennes HS, Lamy CM, Ohning G, Fanselow M et al (2005). Repeated exposure to water avoidance stress in rats: a new model for sustained visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol 289: G42-G53.
6. Célèrier E, Laulin JP, Corcuff JB, Le Moal M, Simonnet G (2001). Progressive enhancement of delayed hyperalgesia induced by repeated heroin administration: a sensitization process. J Neurosci 21: 4074-4080.
7. Célèrier E, Rivat C, Jun Y, Laulin JP, Larcher A, Reynier P et al (2000). Long-lasting hyperalgesia induced by fentanyl in rats: preventive effect of ketamine. Anesthesiology 92: 465-472.
8. Chen L, Huang LY (1991). Sustained potentiation of NMDA receptor-mediated glutamate responses through activation of protein kinase C by a mu opioid. Neuron 7: 319-326.
9. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356: 521-523.
10. Chia YT, Liu K, Wang JJ, Kuo MC, Ho ST (1999). Intraoperative high dose fentanyl induces postoperative fentanyl tolerance. Can J Anaesth 46: 872-877.
11. Crain SM, Shen KF (1990). Opioids can evoke direct receptor-mediated excitatory effects on sensory neurons. Trends Pharmacol Sci 11: 77-81.
12. Crain SM, Shen KF (1998). Modulation of opioid analgesia, tolerance and dependence by Gs-coupled, GM1 ganglioside-regulated opioid receptor functions. Trends Pharmacol Sci 19: 358-365.
13. da Silva Torres IL, Cucco SN, Bassani M, Duarte MS, Silveira PP, Vasconcellos AP et al (2003). Long-lasting delayed hyperalgesia after chronic restraint stress in rats-effect of morphine administration. Neurosci Res 45: 277-283.
14. De Kock M, Lavand'homme P, Waterloos H (2001). Balanced analgesia' in the perioperative period: is there a place for ketamine? Pain 92: 373-380.
15. Galeotti N, Stefano GB, Guarna M, Bianchi E, Ghelardini C (2006). Signaling pathway of morphine induced acute thermal hyperalgesia in mice. Pain 123: 294-305.
16. Gameiro GH, Gameiro PH, Andrade Ada S, Pereira LF, Arthuri MT, Marcondes FK et al (2006). Nociception- and anxiety-like behavior in rats submitted to different periods of restraint stress. Physiol Behav 87: 643-649.
17. Guignard B, Bossard AE, Coste C, Sessler DI, Lebrault C, Alfonsi P et al (2000). Acute opioid tolerance: intraoperative remifentanil increases postoperative pain and morphine requirement. Anesthesiology 93: 409-417.
18. Guignard B, Coste C, Costes H, Sessler DI, Lebrault C, Morris W et al (2002). Supplementing desflurane-remifentanil anesthesia with small-dose ketamine reduces perioperative opioid analgesic requirements. Anesth Analg 95: 103-108, table of contents.
19. Hirbec H, Teilhac J, Kamenka J, Privat A, Vignon J (2000). Binding properties of [3H]gacyclidine(cis(pip/me)-1-[1-(2-thienyl)-2-methylcyclohexyl] piperidine) enantiomers in the rat central nervous system. Brain Res 859: 177-192.
20. Hirota K, Lambert DG (1996). Ketamine: its mechanism(s) of action and unusual clinical uses (editorial). Br J Anaesth 77: 441-444.
21. Hoizey G, Kaltenbach ML, Dukic S, Lamiable D, Millart H, D'Arbigny P et al (2001). Pharmacokinetics of gacyclidine enantiomers in plasma and spinal cord after single enantiomer administration in rats. Int J Pharm 229: 147-153.
22. Kayser V, Guilbaud G (1990). Differential effects of various doses of morphine and naloxone on two nociceptive test thresholds in arthritic and normal rats. Pain 41: 353-363.
23. Khasar SG, Green PG, Levine JD (2005). Repeated sound stress enhances inflammatory pain in the rat. Pain 116: 79-86.
24. Kim DH, Fields HL, Barbaro NM (1990). Morphine analgesia and acute physical dependence: rapid onset of two opposing, dose-related processes. Brain Res 516: 37-40.
25. Laulin JP, Larcher A, Célèrier E, Le Moal M, Simonnet G (1998). Long-lasting increased pain sensitivity in rat following exposure to heroin for the first time. Eur J Neurosci 10: 782-785.
26. Laulin JP, Maurette P, Corcuff JB, Rivat C, Chauvin M, Simonnet G (2002). The role of ketamine in preventing fentanyl-induced hyperalgesia and subsequent acute morphine tolerance. Anesth Analg 94: 1263-1269.
27. Lewis JW, Cannon JT, Liebeskind JC (1980). Opioid and nonopioid mechanisms of stress analgesia. Science 208: 623-625.
28. Mao J (2002). Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. Pain 100: 213-217.
29. Mao J, Price DD, Mayer DJ (1994). Thermal hyperalgesia in association with the development of morphine tolerance in rats: roles of excitatory amino acid receptors and protein kinase C. J Neurosci 14: 2301-2312.
30. Mao J, Sung B, Ji RR, Lim G (2002). Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 22: 8312-8323.
31. Martin WR, Gilbert PE, Jasinski DR, Martin CD (1987). An analysis of naltrexone precipitated abstinence in morphine-dependent chronic spinal dogs. J Pharmacol Exp Ther 240: 565-570.
32. North RA, Williams JT (1976). Enkephalin inhibits firing of myenteric neurones. Nature 264: 460-461.
33. Ossipov MH, Lai J, Vanderah TW, Porreca F (2003). Induction of pain facilitation by sustained opioid exposure: relationship to opioid antinociceptive tolerance. Life Sci 73: 783-800.
34. Perkins FM, Kehlet H (2000). Chronic pain as an outcome of surgery. A review of predictive factors. Anesthesiology 93: 1123-1133.
35. Richebe P, Rivat C, Laulin JP, Maurette P, Simonnet G (2005). Ketamine improves the management of exaggerated postoperative pain observed in perioperative fentanyl-treated rats. Anesthesiology 102: 421-428.
36. Rivat C, Laulin JP, Corcuff JB, Celerier E, Pain L, Simonnet G (2002). Fentanyl enhancement of carrageenan-induced longlasting hyperalgesia in rats: prevention by the N-methyl-D-aspartate receptor antagonist ketamine. Anesthesiology 96: 381-391.
37. Satoh M, Kuraishi Y, Kawamura M (1992). Effects of intrathecal antibodies to substance P, calcitonin gene-related peptide and galanin on repeated cold stress-induced hyperalgesia: comparison with carrageenan-induced hyperalgesia. Pain 49: 273-278.
38. Simonin F, Schmitt M, Laulin JP, Laboureyras E, Jhamandas JH, Mactavish D et al (2006). RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc Natl Acad Sci USA 103: 466-471.
39. Simonnet G, Rivat C (2003). Opioid-induced hyperalgesia: abnormal or normal pain? Neuroreport 14: 1-7.
40. Stubhaug A, Breivik H (1997). Long-term treatment of chronic neuropathic pain with the NMDA (N-methyl-D-aspartate) receptor antagonist ketamine (editorial; comment). Acta Anaesthesiol Scand 41: 329-331.
41. Suarez-Roca H, Silva JA, Arcaya JL, Quintero L, Maixner W, Pinerua-Shuhaibar L (2006). Role of mu-opioid and NMDA receptors in the development and maintenance of repeated swim stress-induced thermal hyperalgesia. Behav Brain Res 167: 205-211.
42. Vanderah TW, Gardell LR, Burgess SE, Ibrahim M, Dogrul A, Zhong CM et al (2000). Dynorphin promotes abnormal pain and spinal opioid antinociceptive tolerance. J Neurosci 20: 7074-7079.
43. Vidal C, Jacob J (1982). Hyperalgesia induced by non-noxious stress in the rat. Neurosci Lett 32: 75-80.
44. Wilder-Smith OH, Arendt-Nielsen L (2006). Postoperative hyperalgesia: its clinical importance and relevance. Anesthesiology 104: 601-607.
45. Woolf CJ, Salter MW (2000). Neuronal plasticity: increasing the gain in pain. Science 288: 1765-1769.
46. Xie JY, Herman DS, Stiller CO, Gardell LR, Ossipov MH, Lai J et al (2005). Cholecystokinin in the rostral ventromedial medulla mediates opioid-induced hyperalgesia and antinociceptive tolerance. J Neurosci 25: 409-416.
47. Zarate E, Sa Rego MM, White PF, Duffy L, Shearer VE, Griffin JD et al (1999). Comparison of adenosine and remifentanil infusions as adjuvants to desflurane anesthesia. Anesthesiology 90: 956-963.