Behavioral and neurochemical analysis of ongoing bone cancer pain in rats

Pain

Volumn 156, Issue 10, 2015, Pages 1864-1873

  Remeniuk, Bethany ^a   Sukhtankar, Devki ^a   Okun, Alec ^b   Navratilova, Edita ^b   Xie, Jennifer Y ^b   King, Tamara ^c   Porreca, Frank ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF NEW ENGLAND   (United States)

Author keywords

Cancer bone pain; Conditioned place preference; Diclofenac; Dopamine release; Morphine; Ongoing pain; Rostral anterior cingulate cortex

Indexed keywords

BETA FUNALTREXAMINE; DICLOFENAC; DOPAMINE; LIDOCAINE; MORPHINE SULFATE; MU OPIATE RECEPTOR; NEUROTRANSMITTER; BETA-FUNALTREXAMINE; LOCAL ANESTHETIC AGENT; MORPHINE; NALTREXONE; NARCOTIC ANALGESIC AGENT; NARCOTIC ANTAGONIST; NONSTEROID ANTIINFLAMMATORY AGENT;

ALLODYNIA; ANALGESIA; ANTERIOR CINGULATE; ARTICLE; BEHAVIOR CHANGE; BONE CANCER; BONE PAIN; BONE REMODELING; CANCER INDUCED BONE PAIN; CANCER PAIN; DOPAMINE RELEASE; MICRODIALYSIS; NOCICEPTIVE PAIN; NUCLEUS ACCUMBENS; PLACE PREFERENCE; PRIORITY JOURNAL; ADENOCARCINOMA; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL BEHAVIOR; BONE TUMOR; CINGULATE GYRUS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; FEMALE; FISCHER 344 RAT; METABOLISM; PAIN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; TUMOR CELL LINE;

ADENOCARCINOMA; ANALGESICS, OPIOID; ANESTHETICS, LOCAL; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BEHAVIOR, ANIMAL; BONE NEOPLASMS; CELL LINE, TUMOR; DICLOFENAC; DISEASE MODELS, ANIMAL; FEMALE; GYRUS CINGULI; LIDOCAINE; MORPHINE; NALTREXONE; NARCOTIC ANTAGONISTS; NUCLEUS ACCUMBENS; PAIN; RATS; RATS, INBRED F344;

EID: 84947722739     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000218     Document Type: Article

References (59)

1. Anonymous. Cancer pain relief and palliative care-report of the WHO expert committee on cancer pain relief and active supportive careintroduction. Who Tech Rep Ser 1990:7-11.
2. Baliki M, Geha P, Fields H, Apkarian A. Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain. Neuron 2010;66:149-60.
3. Becerra L, Borsook D. Signal valence in the nucleus accumbens to pain onset and offset. Eur J Pain 2008;12:866-9.
4. Becerra L, Navratilova E, Porreca F, Borsook D. Analogous responses in the nucleus accumbens and cingulate cortex to pain onset (aversion) and offset (relief) in rats and humans. J Neurophysiol 2013;110: 1221-6.
5. Bennett M, Rayment C, Hjermstad M, Aass N, Caraceni A, Kaasa S. Prevalence and aetiology of neuropathic pain in cancer patients: A systematic review. PAIN 2012;153:359-65.
6. Bennett MI. Cancer pain terminology: Time to develop a taxonomy that promotes good clinical practice and allows research to progress. PAIN 2010;149:426-7.
7. Bloom A, Jimenez-Andrade J, Taylor R, Castaneda-Corral G, Kaczmarska M, Freeman K, Coughlin K, Ghilardi J, Kuskowski M, Mantyh P. Breast cancer-induced bone remodeling, skeletal pain, and sprouting of sensory nerve fibers. J Pain 2011;12:698-711.
8. Cima G. AVMA guidelines for the euthanasia of animal: 2013 edition. Javma-Journal Am Vet Med Assoc 2013;242:715-16.
9. Coleman R. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 2006;12:6243S-9S.
10. De Felice M, Eyde N, Dodick D, Dussor GO, Ossipov MH, Fields HL, Porreca F. Capturing the aversive state of cephalic pain preclinically. Ann Neurol 2013;74:257-65.
11. Dy S, Asch S, Naeim A, Sanati H, Walling A, Lorenz K. Evidence-based standards for cancer pain management. J Clin Oncol 2008;26:3879-85.
12. Falk S, Dickenson AH. Pain and nociception: mechanisms of cancerinduced bone pain. J Clin Oncol 2014;32:1647-54.
13. Fields H. Understanding how opioids contribute to reward and analgesia. Reg Anesth Pain Med 2007;32:242-6.
14. Fields HL. Mu opioid receptor mediated analgesia and reward. In: Pasternak GW, editor. The opiate receptors, Vol. 23: Humana Press, 2011. pp. 239-64.
15. Foley KM. Treatment of cancer-related pain. J Natl Cancer Inst Monogr 2004;32:103-4.
16. Gajda M, Litwin JA, Adriaensen D, Timmermans JP, Cichocki T. Segmental distribution and morphometric features of primary sensory neurons projecting to the tibial periosteum in the rat. Folia Histochem Cytobiol 2004;42:95-9.
17. Honore P, Luger NM, Sabino MA, Schwei MJ, Rogers SD, Mach DB, OKeefe P F, Ramnaraine ML, Clohisy DR, Mantyh PW. Osteoprotegerin blocks bone cancer-induced skeletal destruction, skeletal pain and painrelated neurochemical reorganization of the spinal cord. Nat Med 2000;6: 521-8.
18. Honore P, Rogers S, Schwei M, Salak-Johnson J, Luger N, Sabino M, Clohisy D, Mantyh P. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 2000;98:585-98.
19. Ivanusic JJ. Size, neurochemistry, and segmental distribution of sensory neurons innervating the rat tibia. J Comp Neurol 2009;517:276-83.
20. Jimenez-Andrade JM, Mantyh WG, Bloom AP, Ferng AS, Geffre CP, Mantyh PW. Bone cancer pain. Annals of the New York Academy of Sciences 2010;1198:173-81.
21. Johansen J, Fields H.Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat Neurosci 2004;7:398-403.
22. Johansen JP, Fields HL, Manning BH. The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci U S A 2001;98:8077-82.
23. Kaan TK, Yip PK, Patel S, Davies M, Marchand F, Cockayne DA, Nunn PA, Dickenson AH, Ford AP, Zhong Y, Malcangio M, McMahon SB. Systemic blockade of P2X3 and P2X2/3 receptors attenuates bone cancer pain behaviour in rats. Brain 2010;133:2549-64.
24. King T, Qu C, Okun A, Mercado R, Ren J, Brion T, Lai J, Porreca F. Contribution of afferent pathways to nerve injury-induced spontaneous pain and evoked hypersensitivity. PAIN 2011;152:1997-2005.
25. King T, Vera-Portocarrero L, Gutierrez T, Vanderah T, Dussor G, Lai J, Fields H, Porreca F. Unmasking the tonic-Aversive state in neuropathic pain. Nat Neurosci 2009;12:1364-6.
26. Kroenke K, Theobald D, Wu J, Tu W, Krebs E. Comparative responsiveness of pain measures in cancer patients. J Pain 2012;13: 764-72.
27. Luger N, Mach D, SevcikM, Mantyh P. Bone cancer pain: From model to mechanism to therapy. J Pain Symptom Manage 2005;29:S32-46.
28. Luger NM, Honore P, Sabino MA, Schwei MJ, Rogers SD, Mach DB, Clohisy DR, Mantyh PW. Osteoprotegerin diminishes advanced bone cancer pain. Cancer Res 2001;61:4038-47.
29. Mantyh P. Cancer pain and its impact on diagnosis, survival and quality of life. Nat Rev Neurosci 2006;7:797-809.
30. Mantyh P. Bone cancer pain: Causes, consequences, and therapeutic opportunities. PAIN 2013;154:S54-62.
31. Mao J. Current challenges in translational pain research. Trends Pharmacol Sci 2012;33:568-73.
32. McNicol E, Strassels S, Goudas L, Lau J, Carr D. Nonsteroidal antiinflammatory drugs, alone or combined with opioids, for cancer pain: A systematic review. J Clin Oncol 2004;22:1975-92.
33. Mercadante S, Fulfaro F. World Health Organization guidelines for cancer pain: A reappraisal. Ann Oncol 2005;16:132-5.
34. Mercadante S, Fulfaro F. Management of painful bone metastases. Curr Opin Oncol 2007;19:308-14.
35. Mercadante S, Giarratano A. The long and winding road of non steroidal anti-inflammatory drugs and paracetamol in cancer pain management: A critical review. Crit Rev Oncol Hematol 2013;87:140-5.
36. Montagnini ML, Zaleon CR. Pharmacological management of cancer pain. J Opioid Manag 2009;5:89-96.
37. Mundy G. Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2002;2:584-93.
38. Navratilova E, Xie J, Okun A, Qu C, Eyde N, Ci S, Ossipov M, King T, Fields H, Porreca F. Pain relief produces negative reinforcement through activation of mesolimbic reward-valuation circuitry. Proc Natl Acad Sci U S A 2012;109:20709-13.
39. Navratilova E, Xie JY, King T, Porreca F. Evaluation of reward from pain relief. Ann N Y Acad Sci 2013;1282:1-11.
40. Nersesyan H, Slavin KV. Current approach to cancer pain management: Availability and implications of different treatment options. Ther Clin Risk Manag 2007;3:381-400.
41. Okun A, DeFelice M, Eyde N, Ren J, Mercado R, King T, Porreca F. Transient inflammation-induced ongoing pain is driven by TRPV1 sensitive afferents. Mol Pain 2011;7:4.
42. Okun A, Liu P, Davis P, Ren J, Remeniuk B, Brion T, Ossipov M, Xie J, Dussor G, King T, Porreca F. Afferent drive elicits ongoing pain in a model of advanced osteoarthritis. PAIN 2012;153:924-33.
43. Paice JA, Ferrell B. The management of cancer pain. CA Cancer J Clin 2011;61:157-82.
44. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Elselvier Inc, Burlington, MA, 2007.
45. Percie du Sert N, Rice AS. Improving the translation of analgesic drugs to the clinic: Animal models of neuropathic pain. Br J Pharmacol 2014;1: 2951-63.
46. Porreca F, Ossipov M. Nausea and vomiting side effects with opioid analgesics during treatment of chronic pain: mechanisms, implications, and management options. Pain Med 2009;10:654-62.
47. Portenoy R. Clinical perspectives on preclinical models of bone pain: Questions and promises. PAIN 2011;152:2455-6.
48. Portenoy R. Treatment of cancer pain. Lancet 2011;377:2236-47.
49. QuC, King T, Okun A, Lai J, FieldsH, Porreca F. Lesion of the rostral anterior cingulate cortex eliminates the aversiveness of spontaneous neuropathic pain following partial or complete axotomy. PAIN 2011;152:1641-8.
50. Rainville P, Duncan G, Price D, Carrier B, Bushnell M. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997; 277:968-71.
51. Rice A, Cimino-Brown D, Eisenach J, Kontinen V, Lacroix-Fralish M, Machin I, Mogil J, Stohr T, Consortium PP. Animal models and the prediction of efficacy in clinical trials of analgesic drugs: A critical appraisal and call for uniform reporting standards. PAIN 2008;139:243-7.
52. Roodman G. Mechanisms of disease: mechanisms of bone metastasis. New Engl J Med 2004;350:1655-64.
53. Sabino M, Ghilardi J, Jongen J, Keyser C, Luger N, Mach D, Peters C, Rogers S, Schwei M, de Felipe C, Mantyh P. Simultaneous reduction in cancer pain, bone destruction, and tumor growth by selective inhibition of cyclooxygenase-2. Cancer Res 2002;62:7343-9.
54. Scott DJ, Stohler CS, Egnatuk CM, Wang H, Koeppe RA, Zubieta JK. Placebo and nocebo effects are defined by opposite opioid and dopaminergic responses. Arch Gen Psychiatry 2008;65:220-31.
55. Sterling J, Edwards J, Martin T, Mundy G. Advances in the biology of bone metastasis: how the skeleton affects tumor behavior. Bone 2011;48:6-15.
56. Vierck C, Hansson P, Yezierski R. Clinical and pre-clinical pain assessment: Are we measuring the same thing? PAIN 2008;135:7-10.
57. VolkowN, Li T. Drugs and alcohol: Treating and preventing abuse, addiction and their medical consequences. Pharmacol Ther 2005;108:3-17.
58. Walczak JS, Pichette V, Leblond F, Desbiens K, Beaulieu P. Behavioral, pharmacological and molecular characterization of the saphenous nerve partial ligation: A new model of neuropathic pain. Neuroscience 2005; 132:1093-102.
59. Xie JY, Qu C, Patwardhan A, Ossipov MH, Navratilova E, Becerra L, Borsook D, Porreca F. Activation of mesocorticolimbic reward circuits for assessment of relief of ongoing pain: A potential biomarker of efficacy. PAIN 2014;155:1659-66.