Clinical Review

What Do We Know About Opioid-Induced Hyperalgesia?

Journal of Clinical Outcomes Management. 2014 April;21(4)

References

1. Mao J, Price DD, Mayer DJ. Thermal hyperalgesia in association with the development of morphine tolerance in rats: Roles of excitatory amino acid receptors and protein kinase C. J Neurosci 1994;14:2301–12.

2. Celerier E, Rivat C, Jun Y, et al. Long-lasting hyperalgesia induced by fentanyl in rats: Preventive effect of ketamine. Anesthesiology 2000;92:465–72.

3. Laulin JP, Maurette P, Corcuff JB, et al. The role of ketamine in preventing fentanyl-induced hyperalgesia and subsequent acute morphine tolerance. Anesth Analg 2002;94:1263–9.

4. Lian B, Vera-Portocarrero L, King T, et al. Opioid-induced latent sensitization in a model of non-inflammatory viscerosomatic hypersensitivity. Brain Res 2010;1358:64–70.

5. Hay JL, Kaboutari J, White JM, et al. Model of methadone-induced hyperalgesia in rats and effect of memantine. Eur J Pharmacol 2010;626:229–33.

6. Wala EP, Holtman JR Jr. Buprenorphine-induced hyperalgesia in the rat. Eur J Pharmacol. 2011;651:89–95.

7. Mao J, Sung B, Ji RR, Lim G. Chronic morphine induces downregulation of spinal glutamate transporters: Implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 2002;22:8312–23.

8. Mao J, Sung B, Ji RR, Lim G. Neuronal apoptosis associated with morphine tolerance: Evidence for an opioid-induced neurotoxic mechanism. J Neurosci 2002;22:7650–61.

9. Mao J. Opioid-induced abnormal pain sensitivity. Curr Pain Headache Rep 2006;10:67–70.

10. Woolf CJ. Intrathecal high dose morphine produces hyperalgesia in the rat. Brain Res 1981;209:491–5.

11. Yaksh TL, Harty GJ, Onofrio BM. High dose of spinal morphine produce a nonopiate receptor-mediated hyperesthesia: Clinical and theoretic implications. Anesthesiology 1986;64:590–7.

12. Vanderah TW, Ossipov MH, Lai J, et al. Mechanisms of opioid-induced pain and antinociceptive tolerance: Descending facilitation and spinal dynorphin. Pain 2001;92:5–9.

13. Zhao M, Joo DT. Enhancement of spinal N-methyl-D-aspartate receptor function by remifentanil action at delta-opioid receptors as a mechanism for acute opioid-induced hyperalgesia or tolerance. Anesthesiology 2008;109:308–17.

14. Ghelardini C, Galeotti N, Vivoli E, et al. Molecular interaction in the mouse PAG between NMDA and opioid receptors in morphine-induced acute thermal nociception. J Neurochem 2008;105:91–100.

15. Chen Y, Yang C, Wang ZJ. Ca2+/calmodulin-dependent protein kinase II alpha is required for the initiation and maintenance of opioid-induced hyperalgesia. J Neurosci 2010;30:38–46.

16. Van Elstraete AC, Sitbon P, Mazoit JX, et al. Protective effect of prior administration of magnesium on delayed hyperalgesia induced by fentanyl in rats. Can J Anaesth 2006;53:1180–5.

17. Gu X, Wu X, Liu Y, et al. Tyrosine phosphorylation of the N-methyl-D-aspartate receptor 2B subunit in spinal cord contributes to remifentanil-induced postoperative hyperalgesia: the preventive effect of ketamine. Mol Pain 2009;5:76.

18. Minville V, Fourcade O, Girolami JP, Tack I. Opioid-induced hyperalgesia in a mice model of orthopaedic pain: Preventive effect of ketamine. Br J Anaesth 2010;104:231–8.

19. Cui W, Li Y, Li S, et al. Systemic lidocaine inhibits remifentanil-induced hyperalgesia via the inhibition of cPKCgamma membrane translocation in spinal dorsal horn of rats. J Neurosurg Anesthesiol 2009;21:318–25.

20. Gupta LK, Gupta R, Tripathi CD. N-methyl-D-aspartate receptor modulators block hyperalgesia induced by acute low-dose morphine. Clin Exp Pharmacol Physiol 2011;38:592–7.

21. Bianchi E, Galeotti N, Menicacci C, Ghelardini C. Contribution of G inhibitory protein alpha subunits in paradoxical hyperalgesia elicited by exceedingly low doses of morphine in mice. Life Sci 2011;89:918–25.

22. Ruiz-Medina J, Ledent C, Valverde O. GPR3 orphan receptor is involved in neuropathic pain after peripheral nerve injury and regulates morphine-induced antinociception. Neuropharmacology 2011;61:43–50.

23. Bianchi E, Norcini M, Smrcka A, Ghelardini C. Supraspinal gbetagamma-dependent stimulation of PLCbeta originating from G inhibitory protein-mu opioid receptor-coupling is necessary for morphine induced acute hyperalgesia. J Neurochem 2009;111:171–80.

24. Liang DY, Li X, Clark JD. 5-hydroxytryptamine type 3 receptor modulates opioid-induced hyperalgesia and tolerance in mice. Anesthesiology 2011;114:1180–9.

25. Rivat C, Vera-Portocarrero LP, Ibrahim MM, et al. Spinal NK-1 receptor-expressing neurons and descending pathways support fentanyl-induced pain hypersensitivity in a rat model of postoperative pain. Eur J Neurosci 2009;29:727–37.

26. Vera-Portocarrero LP, Zhang ET, King T, et al. Spinal NK-1 receptor expressing neurons mediate opioid-induced hyperalgesia and antinociceptive tolerance via activation of descending pathways. Pain 2007;129:35–45.

27. Simonin F, Schmitt M, Laulin JP, et al. RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc Natl Acad Sci U S A 2006;103:466–71.

28. Celerier E, Gonzalez JR, Maldonado R, et al. Opioid-induced hyperalgesia in a murine model of postoperative pain: Role of nitric oxide generated from the inducible nitric oxide synthase. Anesthesiology 2006;104:546–55.

29. Vardanyan A, Wang R, Vanderah TW, et al. TRPV1 receptor in expression of opioid-induced hyperalgesia. J Pain 2009;10:243–52.

30. Zhou HY, Chen SR, Chen H, Pan HL. Opioid-induced long-term potentiation in the spinal cord is a presynaptic event. J Neurosci 2010;30:4460–6.

31. Esmaeili-Mahani S, Shimokawa N, Javan M, et al. Low-dose morphine induces hyperalgesia through activation of G alphas, protein kinase C, and L-type ca 2+ channels in rats. J Neurosci Res 2008;86:471–9.

32. Esmaeili-Mahani S, Fereidoni M, Javan M, et al. Nifedipine suppresses morphine-induced thermal hyperalgesia: Evidence for the role of corticosterone. Eur J Pharmacol 2007;567:95–101.

33. Van Elstraete AC, Sitbon P, Mazoit JX, Benhamou D. Gabapentin prevents delayed and long-lasting hyperalgesia induced by fentanyl in rats. Anesthesiology 2008;108:484–94.

34. Van Elstraete AC, Sitbon P, Benhamou D, Mazoit JX. The median effective dose of ketamine and gabapentin in opioid-induced hyperalgesia in rats: An isobolographic analysis of their interaction. Anesth Analg 2011;113:634–40.

35. Wei X, Wei W. Role of gabapentin in preventing fentanyl- and morphine-withdrawal-induced hyperalgesia in rats. J Anesth 2012;26:236–41.

36. Bessiere B, Richebe P, Laboureyras E, Laulin JP, Contarino A, Simonnet G. Nitrous oxide (N2O) prevents latent pain sensitization and long-term anxiety-like behavior in pain and opioid-experienced rats. Neuropharmacology 2007;53:733–40.

37. Hamlin AS, McNally GP, Osborne PB. Induction of c-fos and zif268 in the nociceptive amygdala parallel abstinence hyperalgesia in rats briefly exposed to morphine. Neuropharmacology 2007;53:330–43.

38. Doyle T, Bryant L, Muscoli C, et al. Spinal NADPH oxidase is a source of superoxide in the development of morphine-induced hyperalgesia and antinociceptive tolerance. Neurosci Lett 2010;483:85–9.

39. Liang DY, Liao G, Wang J, et al. A genetic analysis of opioid-induced hyperalgesia in mice. Anesthesiology 2006;104:1054–62.

40. Liang DY, Liao G, Lighthall GK, Peltz G, Clark DJ. Genetic variants of the P-glycoprotein gene Abcb1b modulate opioid-induced hyperalgesia, tolerance and dependence. Pharmacogenet Genomics 2006;16:825–35.

41. Wilson NM, Jung H, Ripsch MS, et al. CXCR4 signaling mediates morphine-induced tactile hyperalgesia. Brain Behav Immun 2011;25:565–73.

42. Terashvili M, Wu HE, Schwasinger E, Tseng LF. Paradoxical hyperalgesia induced by mu-opioid receptor agonist endomorphin-2, but not endomorphin-1, microinjected into the centromedial amygdala of the rat. Eur J Pharmacol 2007;554:137–44.

43. Juni A, Klein G, Pintar JE, Kest B. Nociception increases during opioid infusion in opioid receptor triple knock-out mice. Neuroscience 2007;147:439–44.

44. Waxman AR, Arout C, Caldwell M, et al. Acute and chronic fentanyl administration causes hyperalgesia independently of opioid receptor activity in mice. Neurosci Lett 2009;462:68–72.

45. Juni A, Cai M, Stankova M, et al. Sex-specific mediation of opioid-induced hyperalgesia by the melanocortin-1 receptor. Anesthesiology 2010;112:181–8.

46. Juni A, Klein G, Kowalczyk B, et al. Sex differences in hyperalgesia during morphine infusion: Effect of gonadectomy and estrogen treatment. Neuropharmacology 2008;54:1264–70.

47. Forero M, Chan PS, Restrepo-Garces CE. Successful reversal of hyperalgesia/myoclonus complex with low-dose ketamine infusion. Pain Pract 2012;12:154–8.

48. Vorobeychik Y, Chen L, Bush MC, Mao J. Improved opioid analgesic effect following opioid dose reduction. Pain Med 2008;9:724–7.

49. Cortinas Saenz M, Geronimo Pardo M, Cortinas Saenz ML, et al. Acute opiate tolerance and postoperative hyperalgesia after a brief infusion of remifentanil managed with multimodal analgesia. Rev Esp Anestesiol Reanim 2008;55:40–2.

50. Siniscalchi A, Piraccini E, Miklosova Z, et al. Opioid-induced hyperalgesia and rapid opioid detoxification after tacrolimus administration. Anesth Analg 2008;106:645–6.

51. Okon TR, George ML. Fentanyl-induced neurotoxicity and paradoxic pain. J Pain Symptom Manage 2008;35:327–33.

52. Axelrod DJ, Reville B. Using methadone to treat opioid-induced hyperalgesia and refractory pain. J Opioid Manag 2007;3:113–4.

53. Singler B, Troster A, Manering N, et al. Modulation of remifentanil-induced postinfusion hyperalgesia by propofol. Anesth Analg 2007;104:1397–403.

54. Hallett BR, Chalkiadis GA. Suspected opioid-induced hyperalgesia in an infant. Br J Anaesth 2012;108:116–8.

55. Ma JF, Huang ZL, Li J, et al. Cohort study of remifentanil-induced hyperalgesia in postoperative patients. Zhonghua Yi Xue Za Zhi 2011;91:977–9.

56. Pud D, Cohen D, Lawental E, Eisenberg E. Opioids and abnormal pain perception: New evidence from a study of chronic opioid addicts and healthy subjects. Drug Alcohol Depend 2006;82:218–23.

57. Fishbain DA, Lewis JE, Gao J. Are psychoactive substance (opioid)-dependent chronic pain patients hyperalgesic? Pain Pract 2011;11:337–43.

58. Hay JL, White JM, Bochner F, et al. Hyperalgesia in opioid-managed chronic pain and opioid-dependent patients. J Pain 2009;10:316–22.

59. Chu LF, Clark DJ, Angst MS. Opioid tolerance and hyperalgesia in chronic pain patients after one month of oral morphine therapy: A preliminary prospective study. J Pain 2006;7:43–8.

60. Chu LF, Dairmont J, Zamora AK, et al. The endogenous opioid system is not involved in modulation of opioid-induced hyperalgesia. J Pain 2011;12:108–15.

61. McDonnell C, Zaarour C, Hull R, et al. Pre-treatment with morphine does not prevent the development of remifentanil-induced hyperalgesia. Can J Anaesth 2008;55:813–8.

62. Echevarria G, Elgueta F, Fierro C, et al. Nitrous oxide (N(2)O) reduces postoperative opioid-induced hyperalgesia after remifentanil-propofol anaesthesia in humans. Br J Anaesth 2011;107:959–65.

63. Troster A, Sittl R, Singler B, et al. Modulation of remifentanil-induced analgesia and postinfusion hyperalgesia by parecoxib in humans. Anesthesiology 2006;105:1016–23.

64. Tuncer S, Yalcin N, Reisli R, Alper Y. The effects of lornoxicam in preventing remifentanil-induced postoperative hyperalgesia. Agri 2009;2:161–7.

65. Lee C, Song YK, Jeong HM, Park SN. The effects of magnesium sulfate infiltration on perioperative opioid consumption and opioid-induced hyperalgesia in patients undergoing robot-assisted laparoscopic prostatectomy with remifentanil-based anesthesia. Korean J Anesthesiol 2011;61:244–50.

66. Song JW, Lee YW, Yoon KB, et al. Magnesium sulfate prevents remifentanil-induced postoperative hyperalgesia in patients undergoing thyroidectomy. Anesth Analg 2011;113:390–7.

67. Lee C, Song YK, Lee JH, Ha SM. The effects of intraoperative adenosine infusion on acute opioid tolerance and opioid induced hyperalgesia induced by remifentanil in adult patients undergoing tonsillectomy. Korean J Pain 2011;24:7–12.

68. Hong BH, Lee WY, Kim YH, et al. Effects of intraoperative low dose ketamine on remifentanil-induced hyperalgesia in gynecologic surgery with sevoflurane anesthesia. Korean J Anesthesiol 2011;61:238–43.

69. Xuerong Y, Yuguang H, Xia J, Hailan W. Ketamine and lornoxicam for preventing a fentanyl-induced increase in postoperative morphine requirement. Anesth Analg 2008;107:2032–7.

70. Schlimp CJ, Pipam W, Wolrab C, Ohner C, Kager HI, Likar R. Clonidine for remifentanil-induced hyperalgesia: A double-blind randomized, placebo-controlled study of clonidine under intra-operative use of remifentanil in elective surgery of the shoulder. Schmerz 2011;25:290–5.

71. Belgrade M, Hall S. Dexmedetomidine infusion for the management of opioid-induced hyperalgesia. Pain Med 2010;11:1819–26.

72. Chen L, Malarick C, Seefeld L, et al. Altered quantitative sensory testing outcome in subjects with opioid therapy. Pain 2009;143:65–70.

73. Bannister K, Dickenson AH. Opioid hyperalgesia. Curr Opin Support Palliat Care 2010;4:1–5.

74. Ram KC, Eisenberg E, Haddad M, Pud D. Oral opioid use alters DNIC but not cold pain perception in patients with chronic pain - new perspective of opioid-induced hyperalgesia. Pain 2008;139:431–8.

75. Compton P, Charuvastra VC, Ling W. Pain intolerance in opioid-maintained former opiate addicts: Effect of long-acting maintenance agent. Drug Alcohol Depend 2001;63:139–46.

76. Vinik HR, Kissin I. Rapid development of tolerance to analgesia during remifentanil infusion in humans. Anesth Analg 1998;86:1307–11.

77. Mao J, Price DD, Mayer DJ. Mechanisms of hyperalgesia and morphine tolerance: A current view of their possible interactions. Pain 1995;62:259–74.

78. Sjogren P, Jensen NH, Jensen TS. Disappearance of morphine-induced hyperalgesia after discontinuing or substituting morphine with other opioid agonists. Pain 1994;59:313–6.

79. Guignard B, Bossard AE, Coste C, et al. Acute opioid tolerance: Intraoperative remifentanil increases postoperative pain and morphine requirement. Anesthesiology 2000;93:409–17.

80. Angst MS, Clark JD. Opioid-induced hyperalgesia: A qualitative systematic review. Anesthesiology 2006;104:570–87.

81. Baron MJ, McDonald PW. Significant pain reduction in chronic pain patients after detoxification from high-dose opioids. J Opioid Manag 2006;2:277–82

82. Mao J. Opioid-induced abnormal pain sensitivity: Implications in clinical opioid therapy. Pain 2002;100:213–7.

83. Low Y, Clarke CF, Huh BK. Opioid-induced hyperalgesia: A review of epidemiology, mechanisms and management. Singapore Med J 2012;53:357–60.

84. Fishbain DA, Cole B, Lewis JE, et al. Do opioids induce hyperalgesia in humans? An evidence-based structured review. Pain Med 2009:829–39.

85. Chu LF, D’Arcy N, Brady C, et al. Analgesic tolerance without demonstrable opioid-induced hyperalgesia: a double-blinded, randomized, placebo-controlled trial of sustained-release morphine for treatment of chronic nonradicular low-back pain. Pain 2012;153:1583–92.