Imaging opioid analgesia in the human brain

Trends in Anaesthesia and Critical Care

Volumn 2, Issue 5, 2012, Pages 244-248

  Lee, Michael C ^a   Wanigasekera, Vishvarani ^a   Tracey, Irene ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

FMRI; Neuroimaging; Opioids; Pain; PET

Indexed keywords

OPIATE; OPIATE RECEPTOR;

ANALGESIA; DRUG TOLERANCE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPERALGESIA; LIMBIC CORTEX; LONG TERM CARE; NEUROIMAGING; NONHUMAN; OPIATE ADDICTION; PAIN; PALLIATIVE THERAPY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW;

EID: 84867230075     PISSN: 22108440     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tacc.2012.07.002     Document Type: Review

References (106)

1. Mogil J.S. Animal models of pain: progress and challenges. Nat Rev Neurosci 2009, 10(4):283-294.
2. Wu C.L., Raja S.N. Treatment of acute postoperative pain. Lancet 2011, 377(9784):2215-2225.
3. Portenoy R.K. Treatment of cancer pain. Lancet 2011, 377(9784):2236-2247.
4. Chou R., Ballantyne J.C., Fanciullo G.J., Fine P.G., Miaskowski C. Research gaps on use of opioids for chronic noncancer pain: findings from a review of the evidence for an American pain society and American academy of pain medicine clinical practice guideline. J Pain 2009, 10(2):147-159.
5. Noble M., Treadwell J.R., Tregear S.J., Coates V.H., Wiffen P.J., Akafomo C., et al. Long-term opioid management for chronic noncancer pain. Cochrane Database Syst Rev 2010, 1:CD006605.
6. Okie S. A flood of opioids, a rising tide of deaths. N Engl J Med 2010, 363(21). 1981-5.
7. Opioids for persistent pain: good practice 2010, British Pain Society.
8. Chou R., Fanciullo G.J., Fine P.G., Adler J.A., Ballantyne J.C., Davies P., et al. Clinical guidelines for the use of chronic opioid therapy in chronic noncancer pain. J Pain 2009, 10(2):113-130.
9. Kahan M., Mailis-Gagnon A., Wilson L., Srivastava A. Canadian guideline for safe and effective use of opioids for chronic noncancer pain: clinical summary for family physicians. Part 1: general population. Can Fam Physician 2011, 57(11):1257-1266. e407-18.
10. Kahan M., Wilson L., Mailis-Gagnon A., Srivastava A. Canadian guideline for safe and effective use of opioids for chronic noncancer pain: clinical summary for family physicians. Part 2: special populations. Can Fam Physician 2011, 57(11):1269-1276. e419-28.
11. Stein C., Lang L.J. Peripheral mechanisms of opioid analgesia. Curr Opin Pharmacol 2009, 9(1):3-8.
12. Ossipov M.H., Lai J., King T., Vanderah T.W., Malan T.P., Hruby V.J., et al. Antinociceptive and nociceptive actions of opioids. J Neurobiol 2004, 61(1):126-148.
13. Thomas J., Karver S., Cooney G.A., Chamberlain B.H., Watt C.K., Slatkin N.E., et al. Methylnaltrexone for opioid-induced constipation in advanced illness. N Engl J Med 2008, 358(22):2332-2343.
14. Michna E., Blonsky E.R., Schulman S., Tzanis E., Manley A., Zhang H., et al. Subcutaneous methylnaltrexone for treatment of opioid-induced constipation in patients with chronic, nonmalignant pain: a randomized controlled study. J Pain 2011, 12(5):554-562.
15. Adler L.J., Gyulai F.E., Diehl D.J., Mintun M.A., Winter P.M., Firestone L.L. Regional brain activity changes associated with fentanyl analgesia elucidated by positron emission tomography. Anesth Analg 1997, 84(1):120-126.
16. Petrovic P., Kalso E., Petersson K.M., Ingvar M. Placebo and opioid analgesia-; imaging a Shared neuronal Network. Science 2002, 295(5560):1737-1740.
17. Becerra L., Harter K., Gonzalez R.G., Borsook D. Functional magnetic resonance imaging measures of the effects of morphine on central nervous system circuitry in opioid-naive healthy volunteers. Anesth Analg 2006, 103(1):208-216. [table of contents].
18. Wagner K.J., Sprenger T., Kochs E.F., Tolle T.R., Valet M., Willoch F. Imaging human cerebral pain modulation by dose-dependent opioid analgesia: a positron emission tomography activation study using remifentanil. Anesthesiology 2007, 106(3):548-556.
19. Wise R.G., Rogers R., Painter D., Bantick S., Ploghaus A., Williams P., et al. Combining fMRI with a pharmacokinetic model to determine which brain areas activated by painful stimulation are specifically modulated by remifentanil. Neuroimage 2002, 16(4):999-1014.
20. Oertel B.G., Preibisch C., Wallenhorst T., Hummel T., Geisslinger G., Lanfermann H., et al. Differential opioid action on sensory and affective cerebral pain processing. Clin Pharmacol Ther 2008, 83(4):577-588.
21. Upadhyay J., Anderson J., Baumgartner R., Coimbra A., Schwarz A.J., Pendse G., et al. Modulation of CNS pain circuitry by intravenous and sublingual doses of buprenorphine. Neuroimage 2012, 59(4):3762-3773.
22. Wise R.G., Williams P., Tracey I. Using fMRI to quantify the time dependence of remifentanil analgesia in the human brain. Neuropsychopharmacology 2004, 29(3):626-635.
23. Pattinson K.T., Rogers R., Mayhew S.D., Tracey I., Wise R.G. Pharmacological FMRI: measuring opioid effects on the BOLD response to hypercapnia. J Cereb Blood Flow Metab 2007, 27(2):414-423.
24. Zubieta J.K., Smith Y.R., Bueller J.A., Xu Y., Kilbourn M.R., Jewett D.M., et al. Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science 2001, 293(5528):311-315.
25. Bencherif B., Fuchs P.N., Sheth R., Dannals R.F., Campbell J.N., Frost J.J. Pain activation of human supraspinal opioid pathways as demonstrated by [11C]-carfentanil and positron emission tomography (PET). Pain 2002, 99(3):589-598.
26. Sprenger T., Valet M., Boecker H., Henriksen G., Spilker M.E., Willoch F., et al. Opioidergic activation in the medial pain system after heat pain. Pain 2006, 122(1-2):63-67.
27. Scott D.J., Stohler C.S., Egnatuk C.M., Wang H., Koeppe R.A., Zubieta J.K. Placebo and nocebo effects are defined by opposite opioid and dopaminergic responses. Arch Gen Psychiatry 2008, 65(2):220-231.
28. Bingel U., Wanigasekera V., Wiech K., Ni Mhuircheartaigh R., Lee M.C., Ploner M., et al. The effect of treatment expectation on drug efficacy: imaging the analgesic benefit of the opioid remifentanil. Sci Transl Med 2011, 3(70):70ra14.
29. Jones A.K., Cunningham V.J., Ha-Kawa S., Fujiwara T., Luthra S.K., Silva S., et al. Changes in central opioid receptor binding in relation to inflammation and pain in patients with rheumatoid arthritis. Br J Rheumatol 1994, 33(10):909-916.
30. Willoch F., Schindler F., Wester H.J., Empl M., Straube A., Schwaiger M., et al. Central poststroke pain and reduced opioid receptor binding within pain processing circuitries: a [11C] diprenorphine PET study. Pain 2004, 108(3):213-220.
31. Jones A.K., Watabe H., Cunningham V.J., Jones T. Cerebral decreases in opioid receptor binding in patients with central neuropathic pain measured by [11C] diprenorphine binding and PET. Eur J Pain 2004, 8(5):479-485.
32. Maarrawi J., Peyron R., Mertens P., Costes N., Magnin M., Sindou M., et al. Differential brain opioid receptor availability in central and peripheral neuropathic pain. Pain 2007, 127(1-2):183-194.
33. Harris R.E., Clauw D.J., Scott D.J., McLean S.A., Gracely R.H., Zubieta J.K. Decreased central mu-opioid receptor availability in fibromyalgia. J Neurosci 2007, 27(37):10000-10006.
34. Klega A., Eberle T., Buchholz H.G., Maus S., Maihofner C., Schreckenberger M., et al. Central opioidergic neurotransmission in complex regional pain syndrome. Neurology 2010, 75(2):129-136.
35. Henriksen G., Willoch F. Imaging of opioid receptors in the central nervous system. Brain 2008, 131(Pt 5):1171-1196.
36. Melichar J.K., Hume S.P., Williams T.M., Daglish M.R., Taylor L.G., Ahmad R., et al. Using [11C] diprenorphine to image opioid receptor occupancy by methadone in opioid addiction: clinical and preclinical studies. J Pharmacol Exp Ther 2005, 312(1):309-315.
37. Nagi K., Pineyro G. Regulation of opioid receptor signalling: implications for the development of analgesic tolerance. Mol Brain 2011, 4:25.
38. Vaccarino A.L., Marek P., Kest B., Ben-Eliyahu S., Couret L.C., Kao B., et al. Morphine fails to produce tolerance when administered in the presence of formalin pain in rats. Brain Res 1993, 627(2):287-290.
39. Zollner C., Mousa S.A., Fischer O., Rittner H.L., Shaqura M., Brack A., et al. Chronic morphine use does not induce peripheral tolerance in a rat model of inflammatory pain. J Clin Invest 2008, 118(3):1065-1073.
40. Urch C.E., Donovan-Rodriguez T., Gordon-Williams R., Bee L.A., Dickenson A.H. Efficacy of chronic morphine in a rat model of cancer-induced bone pain: behavior and in dorsal horn pathophysiology. J Pain 2005, 6(12):837-845.
41. Iwai S., Kiguchi N., Kobayashi Y., Fukazawa Y., Saika F., Ueno K., et al. Inhibition of morphine tolerance is mediated by painful stimuli via central mechanisms. Drug Discov Ther 2012, 6(1):31-37.
42. Raghavendra V., Rutkowski M.D., DeLeo J.A. The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J Neurosci 2002, 22(22):9980-9989.
43. Simonnet G., Rivat C. Opioid-induced hyperalgesia: abnormal or normal pain?. Neuroreport 2003, 14(1):1-7.
44. Muscoli C., Doyle T., Dagostino C., Bryant L., Chen Z., Watkins L.R., et al. Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J Neurosci 2010, 30(46):15400-15408.
45. Waxman A.R., Arout C., Caldwell M., Dahan A., Kest B. Acute and chronic fentanyl administration causes hyperalgesia independently of opioid receptor activity in mice. Neurosci Lett 2009, 462(1):68-72.
46. van Dorp E.L., Kest B., Kowalczyk W.J., Morariu A.M., Waxman A.R., Arout C.A., et al. Morphine-6beta-glucuronide rapidly increases pain sensitivity independently of opioid receptor activity in mice and humans. Anesthesiology 2009, 110(6):1356-1363.
47. Tompkins D.A., Campbell C.M. Opioid-induced hyperalgesia: clinically relevant or extraneous research phenomenon?. Curr Pain Headache Rep 2011, 15(2):129-136.
48. Baron M.J., McDonald P.W. Significant pain reduction in chronic pain patients after detoxification from high-dose opioids. J Opioid Manag 2006, 2(5):277-282.
49. Bannister K., Dickenson A.H. Opioid hyperalgesia. Curr Opin Support Palliat Care 2010, 4(1):1-5.
50. Heinl C., Drdla-Schutting R., Xanthos D.N., Sandkuhler J. Distinct mechanisms underlying pronociceptive effects of opioids. J Neurosci 2011, 31(46):16748-16756.
51. 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(3):218-223.
52. Compton P., Charuvastra V.C., Kintaudi K., Ling W. Pain responses in methadone-maintained opioid abusers. J Pain Symptom Manage 2000, 20(4):237-245.
53. Doverty M., White J.M., Somogyi A.A., Bochner F., Ali R., Ling W. Hyperalgesic responses in methadone maintenance patients. Pain 2001, 90(1-2):91-96.
54. Cooper Z.D., Sullivan M.A., Vosburg S.K., Manubay J.M., Haney M., Foltin R.W., et al. Effects of repeated oxycodone administration on its analgesic and subjective effects in normal, healthy volunteers. Behav Pharmacol 2012.
55. Angst M.S., Clark J.D. Opioid-induced hyperalgesia: a qualitative systematic review. Anesthesiology 2006, 104(3):570-587.
56. Luginbuhl M., Gerber A., Schnider T.W., 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(3):726-732. [table of contents].
57. Jensen K.B., Lonsdorf T.B., Schalling M., Kosek E., Ingvar M. Increased sensitivity to thermal pain following a single opiate dose is influenced by the COMT val(158)met polymorphism. PLoS ONE 2009, 4(6):e6016.
58. Wanigasekera V., Lee M.C., Rogers R., Hu P., Tracey I. Neural correlates of an injury-free model of central sensitization induced by opioid withdrawal in humans. J Neurosci 2011, 31(8):2835-2842.
59. Petersen K.L., Jones B., Segredo V., Dahl J.B., Rowbotham M.C. Effect of remifentanil on pain and secondary hyperalgesia associated with the heat-capsaicin sensitization model in healthy volunteers. Anesthesiology 2001, 94(1):15-20.
60. Angst M.S., Koppert W., Pahl I., Clark D.J., Schmelz M. Short-term infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 2003, 106(1-2):49-57.
61. Kaplan H., Fields H.L. Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla. J Neurosci 1991, 11(5):1433-1439.
62. Koob G.F., Maldonado R., Stinus L. Neural substrates of opiate withdrawal. Trends Neurosci 1992, 15(5):186-191.
63. Bozarth M.A., Wise R.A. Anatomically distinct opiate receptor fields mediate reward and physical dependence. Science 1984, 224(4648):516-517.
64. Li X., Angst M.S., Clark J.D. Opioid-induced hyperalgesia and incisional pain. Anesth Analg 2001, 93(1):204-209.
65. Liang D., Shi X., Qiao Y., Angst M.S., Yeomans D.C., Clark J.D. Chronic morphine administration enhances nociceptive sensitivity and local cytokine production after incision. Mol Pain 2008, 4:7.
66. Celerier E., Gonzalez J.R., Maldonado R., Cabanero D., Puig M.M. Opioid-induced hyperalgesia in a murine model of postoperative pain: role of nitric oxide generated from the inducible nitric oxide synthase. Anesthesiology 2006, 104(3):546-555.
67. Rivat C., Vera-Portocarrero L.P., Ibrahim M.M., Mata H.P., Stagg N.J., De Felice M., 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(4):727-737.
68. King T., Vardanyan A., Majuta L., Melemedjian O., Nagle R., Cress A.E., et al. Morphine treatment accelerates sarcoma-induced bone pain, bone loss, and spontaneous fracture in a murine model of bone cancer. Pain 2007, 132(1-2):154-168.
69. Guignard B., Bossard A.E., Coste C., Sessler D.I., Lebrault C., Alfonsi P., et al. Acute opioid tolerance: intraoperative remifentanil increases postoperative pain and morphine requirement. Anesthesiology 2000, 93(2):409-417.
70. Rauf K., Vohra A., Fernandez-Jimenez P., O'Keeffe N., Forrest M. Remifentanil infusion in association with fentanyl-propofol anaesthesia in patients undergoing cardiac surgery: effects on morphine requirement and postoperative analgesia. Br J Anaesth 2005, 95(5):611-615.
71. Cortinez L.I., Brandes V., Munoz H.R., Guerrero M.E., Mur M. No clinical evidence of acute opioid tolerance after remifentanil-based anaesthesia. Br J Anaesth 2001, 87(6):866-869.
72. Lee L.H., Irwin M.G., Lui S.K. Intraoperative remifentanil infusion does not increase postoperative opioid consumption compared with 70% nitrous oxide. Anesthesiology 2005, 102(2):398-402.
73. Fishbain D.A., Cole B., Lewis J.E., Gao J., Rosomoff R.S. Do opioids induce hyperalgesia in humans? An evidence-based structured review. Pain Med 2009, 10(5):829-839.
74. Chen L., Malarick C., Seefeld L., Wang S., Houghton M., Mao J. Altered quantitative sensory testing outcome in subjects with opioid therapy. Pain 2009, 143(1-2):65-70.
75. Chu L.F., Clark D.J., Angst M.S. Opioid tolerance and hyperalgesia in chronic pain patients after one month of oral morphine therapy: a preliminary prospective study. J Pain 2006, 7(1):43-48.
76. Reznikov I., Pud D., Eisenberg E. Oral opioid administration and hyperalgesia in patients with cancer or chronic nonmalignant pain. Br J Clin Pharmacol 2005, 60(3):311-318.
77. Dhalla I.A., Persaud N., Juurlink D.N. Facing up to the prescription opioid crisis. BMJ 2011, 343:d5142.
78. Weissman D.E., Haddox J.D. Opioid pseudoaddiction-an iatrogenic syndrome. Pain 1989, 36(3):363-366.
79. Turk D.C., Swanson K.S., Gatchel R.J. Predicting opioid misuse by chronic pain patients: a systematic review and literature synthesis. Clin J Pain 2008, 24(6):497-508.
80. Webster L.R., Cochella S., Dasgupta N., Fakata K.L., Fine P.G., Fishman S.M., et al. An analysis of the root causes for opioid-related overdose deaths in the United States. Pain Med 2011, 12(Suppl. 2):S26-S35.
81. Braden J.B., Russo J., Fan M.Y., Edlund M.J., Martin B.C., DeVries A., et al. Emergency department visits among recipients of chronic opioid therapy. Arch Intern Med 2010, 170(16):1425-1432.
82. Fields HL. The doctor's dilemma: opiate analgesics and chronic pain. Neuron. 69(4): 591-594.
83. Bell K., Salmon A. Pain, physical dependence and pseudoaddiction: redefining addiction for 'nice' people?. Int J Drug Policy 2009, 20(2):170-178.
84. Leknes S., Lee M., Berna C., Andersson J., Tracey I. Relief as a reward: hedonic and neural responses to safety from pain. PLoS ONE 2011, 6(4):e17870.
85. Gardner E.L. What we have learned about addiction from animal models of drug self-administration. Am J Addictions/Am Acad Psychiatr Alcoholism Addictions 2000, 9(4):285-313.
86. Weeks J.R. Experimental morphine addiction: method for automatic intravenous injections in unrestrained rats. Science 1962, 138(3537):143-144.
87. Lyness W.H., Smith F.L., Heavner J.E., Iacono C.U., Garvin R.D. Morphine self-administration in the rat during adjuvant-induced arthritis. Life Sci 1989, 45(23):2217-2224.
88. Colpaert F.C., Meert T., De Witte P., Schmitt P. Further evidence validating adjuvant arthritis as an experimental model of chronic pain in the rat. Life Sci 1982, 31(1):67-75.
89. Colpaert F.C., Tarayre J.P., Alliaga M., Bruins Slot L.A., Attal N., Koek W. Opiate self-administration as a measure of chronic nociceptive pain in arthritic rats. Pain 2001, 91(1-2):33-45.
90. Ozaki S., Narita M., Narita M., Iino M., Miyoshi K., Suzuki T. Suppression of the morphine-induced rewarding effect and G-protein activation in the lower midbrain following nerve injury in the mouse: involvement of G-protein-coupled receptor kinase 2. Neuroscience 2003, 116(1):89-97.
91. Ozaki S., Narita M., Ozaki M., Khotib J., Suzuki T. Role of extracellular signal-regulated kinase in the ventral tegmental area in the suppression of the morphine-induced rewarding effect in mice with sciatic nerve ligation. J Neurochem 2004, 88(6):1389-1397.
92. Narita M., Kishimoto Y., Ise Y., Yajima Y., Misawa K., Suzuki T. Direct evidence for the involvement of the mesolimbic kappa-opioid system in the morphine-induced rewarding effect under an inflammatory pain-like state. Neuropsychopharmacology 2005, 30(1):111-118.
93. Conley K.M., Toledano A.Y., Apfelbaum J.L., Zacny J.P. Modulating effects of a cold water stimulus on opioid effects in volunteers. Psychopharmacology (Berl) 1997, 131(4):313-320.
94. Zacny J.P., McKay M.A., Toledano A.Y., Marks S., Young C.J., Klock P.A., et al. The effects of a cold-water immersion stressor on the reinforcing and subjective effects of fentanyl in healthy volunteers. Drug Alcohol Depend 1996, 42(2):133-142.
95. Lasagna L., Von Felsinger J.M., Beecher H.K. Drug-induced mood changes in man. I. Observations on healthy subjects, chronically ill patients, and postaddicts. J Am Med Assoc 1955, 157(12):1006-1020.
96. Azolosa J.L., Stitzer M.L., Greenwald M.K. Opioid physical dependence development: effects of single versus repeated morphine pretreatments and of subjects' opioid exposure history. Psychopharmacology (Berl) 1994, 114(1):71-80.
97. Samaha A.N., Robinson T.E. Why does the rapid delivery of drugs to the brain promote addiction?. Trends Pharmacol Sci 2005, 26(2):82-87.
98. Marsch L.A., Bickel W.K., Badger G.J., Rathmell J.P., Swedberg M.D., Jonzon B., et al. Effects of infusion rate of intravenously administered morphine on physiological, psychomotor, and self-reported measures in humans. J Pharmacol Exp Ther 2001, 299(3):1056-1065.
99. Comer S.D., Ashworth J.B., Sullivan M.A., Vosburg S.K., Saccone P.A., Foltin R.W. Relationship between rate of infusion and reinforcing strength of oxycodone in humans. J Opioid Manag 2009, 5(4):203-212.
100. Comer S.D., Sullivan M.A., Vosburg S.K., Kowalczyk W.J., Houser J. Abuse liability of oxycodone as a function of pain and drug use history. Drug Alcohol Depend 2010, 109(1-3):130-138.
101. Firestone L.L., Gyulai F., Mintun M., Adler L.J., Urso K., Winter P.M. Human brain activity response to fentanyl imaged by positron emission tomography. Anesth Analg 1996, 82(6):1247-1251.
102. Leppa M., Korvenoja A., Carlson S., Timonen P., Martinkauppi S., Ahonen J., et al. Acute opioid effects on human brain as revealed by functional magnetic resonance imaging. Neuroimage 2006, 31(2):661-669.
103. Schmidt-Wilcke T. Variations in brain volume and regional morphology associated with chronic pain. Curr Rheumatol Rep 2008, 10(6):467-474.
104. Younger J.W., Chu L.F., D'Arcy N.T., Trott K.E., Jastrzab L.E., Mackey S.C. Prescription opioid analgesics rapidly change the human brain. Pain 2011, 152(8):1803-1810.
105. Baliki M.N., Geha P.Y., Fields H.L., Apkarian A.V. Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain. Neuron 2010, 66(1):149-160.
106. Leknes S., Tracey I. A common neurobiology for pain and pleasure. Nat Rev Neurosci 2008, 9(4):314-320.