The conditioned place preference test for assessing welfare consequences and potential refinements in a mouse bladder cancer model

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Roughan, John V ^a   Coulter, Claire A ^a   Flecknell, Paul A ^a   Thomas, Huw D ^a   Sufka, Kenneth J ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHINE; ANALGESIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL WELFARE; ARTICLE; BEHAVIOR CHANGE; BLADDER CANCER; CANCER MODEL; CANCER PAIN; CONDITIONED PLACE PREFERENCE TEST; CONTROLLED STUDY; EUTHANASIA; FEMALE; HARGREAVES TEST; HYPERALGESIA; MALAISE; MOUSE; MOUSE MODEL; NONHUMAN; PAIN THRESHOLD; TUMOR VOLUME; WEIGHT CHANGE; ANIMAL; ANIMAL BEHAVIOR; EXPERIMENTAL NEOPLASM; PAIN; PATHOLOGY; PATHOPHYSIOLOGY; PRECLINICAL STUDY; PROCEDURES; URINARY BLADDER NEOPLASMS;

ANALGESICS; ANIMALS; BEHAVIOR, ANIMAL; DRUG EVALUATION, PRECLINICAL; FEMALE; HYPERALGESIA; MICE; NEOPLASMS, EXPERIMENTAL; PAIN; URINARY BLADDER NEOPLASMS;

EID: 84905455177     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103362     Document Type: Article

References (79)

1. Cowan A, Doxey JC, Harry EJ (1977) The animal pharmacology of buprenorphine, an oripavine analgesic agent. Br J Pharmacol 60: 547-554. (Pubitemid 8149540)
2. Dennis SG, Melzack R (1979) Comparison of phasic and tonic pain in animals. In: Bonica JJ, editor. Advances in pain research and therapy. New York: Raven Press. 747-760.
3. Mogil JS, Crager SE (2004) What should we be measuring in behavioral studies of chronic pain in animals. Pain 112: 12-15. (Pubitemid 39371015)
4. Sufka K (2011) Translational challenges and analgesic screening assays. Pain 152: 1942-1943.
5. Mao J (2012) Current challenges in translational pain research. Trends Pharmacol Sci 33: 568-573.
6. Duncan IJH (1996) Animal welfare defined in terms of feelings. Acta Agriculturae Scandinavica Section A-Animal Science Supplementum 27: 29-35.
7. Flecknell P, Leach M, Bateson M (2011) Affective state and quality of life in mice. Pain 152: 963-964.
8. Mendl M, Burman OHP, Parker RMA, Paul ES (2009) Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Appl Anim Behav Sci 118: 161-181.
9. HMSO (2012) Statistics of Scientific Procedures on Living Animals (Great Britain). London: Her Majesty's Stationary Office.
10. UKCCCR (1998) United Kingdom Co-ordinating Committee on Cancer Research (UKCCCR) Guidelines for the Welfare of Animals in Experimental Neoplasia (Second Edition). Br J Cancer 77: 1-10.
11. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, et al. (2010) Guidelines for the welfare and use of animals in cancer research. Br J Cancer 102: 1555-1577.
12. Asai H, Ozaki N, Shinoda M, Nagamine K, Tohnai I, et al. (2005) Heat and mechanical hyperalgesia in mice model of cancer pain. Pain 117: 19-29. (Pubitemid 41764769)
13. Fox A, Medhurst S, Courade JP, Glatt M, Dawson J, et al. (2004) Antihyperalgesic activity of the cox-2 inhibitor lumiracoxib in a model of bone cancer pain in the rat. Pain 107: 33-40. (Pubitemid 38058696)
14. Lee BH, Seong J, Kim UJ, Won R, Kim M (2005) Behavioral characteristics of a mouse model of cancer pain. Yonsei Med J 46: 252-259. (Pubitemid 40662979)
15. Zhang HW, Iida Y, Andoh T, Nojima H, Murata J, et al. (2003) Mechanical hypersensitivity and alterations in cutaneous nerve fibers in a mouse model of skin cancer pain. J Pharmacol Sci 91: 167-170. (Pubitemid 36575570)
16. Calixto-Campos C, Zarpelon AC, Correa M, Cardoso RDR, Pinho-Ribeiro FA, et al. (2013) The Ehrlich tumor induces pain-like behavior in mice: a novel model of cancer pain for pathophysiological studies and pharmacological screening. BioMed Res Int 2013: 624815.
17. Hang L-H, Shao D-H, Chen Z, Chen Y-F, Shu W-W, et al. (2013) Involvement of spinal CC chemokine ligand 5 in the development of bone cancer pain in rats. Basic Clin Pharmacol Toxicol 113: 325-328.
18. Liu M, Yang H, Fang D, Yang J-J, Cai J, et al. (2013) Upregulation of P263 receptors by neuronal calcium sensor protein VILIP-1 in dorsal root ganglions contributes to the bone cancer pain in rats. Pain 154: 1551-1568.
19. Zhao J, Zhang H, Liu SB, Han P, Hu S, et al. (2013) Spinal interleukin-33 and its receptor ST2 contribute to bone cancer-induced pain in mice. Neurosci 253: 172-182.
20. Leach MC, Allweiler S, Richardson C, Roughan JV, Narbe R, et al. (2009) Behavioural effects of ovariohysterectomy and oral administration of meloxicam in laboratory housed rabbits. Res Vet Sci 87: 336-347.
21. Roughan JV, Flecknell PA (2001) Behavioural effects of laparotomy and analgesic effects of ketoprofen and carprofen in rats. Pain 90: 65-74. (Pubitemid 32146558)
22. Roughan JV, Flecknell PA (2003) Validation of a behaviour-based postoperative pain-scoring system in rats. Proceedings of the Association of Veterinary Anaesthetists Spring Meeting, Dublin 2002. Vet Anaesth Analg 30: 54.
23. Roughan JV, Flecknell PA (2003) Evaluation of a short duration behaviour-based post-operative pain scoring system in rats. Eur J Pain 7: 397-406. (Pubitemid 37101779)
24. Roughan JV, Flecknell PA (2006) Training in behaviour-based post-operative pain scoring in rats - An evaluation based on improved recognition of analgesic requirements. Appl Anim Behav Sci 96: 327-342. (Pubitemid 43162364)
25. Roughan JV, Flecknell PA, Orr HE (2003) Behavioural assessment of postoperative pain and analgesic effects of carprofen in the domestic rabbit. 8th World Congress of Veterinary Anaesthesia. Knoxville, USA. 143.
26. Wright-Williams SL, Courade J-P, Richardson CA, Roughan JV, Flecknell PA (2007) Effects of vasectomy surgery and meloxicam treatment on faecal corticosterone levels and behaviour in two strains of laboratory mouse. Pain 130: 108-118. (Pubitemid 46843457)
27. Roughan JV, Wright-Williams SL, Flecknell PA (2009) Automated analysis of postoperative behaviour: assessment of HomeCageScan as a novel method to rapidly identify pain and analgesic effects in mice. Lab Anim 43: 17-26.
28. Miller AL, Flecknell PA, Leach MC, Roughan JV (2011) A comparison of a manual and an automated behavioural analysis method for assessing postoperative pain in mice. Appl Anim Behav Sci 131: 138-144.
29. Dickinson AL, Leach MC, Flecknell PA (2009) The analgesic effects of oral paracetamol in two strains of mice undergoing vasectomy. Lab Anim 43: 357-361.
30. Miller AL, Wright-Williams SL, Flecknell PA, Roughan JV (2012) A comparison of abdominal and scrotal approach methods of vasectomy and the influence of analgesic treatment in laboratory mice. Lab Anim 46: 304-310.
31. Wright-Williams S, Flecknell PA, Roughan JV (2013) Comparative effects of vasectomy surgery and buprenorphine treatment on faecal corticosterone concentrations and behaviour assessed by manual and automated analysis methods in C57 and C3H mice. PLoS ONE [Electronic Resource] 8: e75948.
32. Vermeirsch H, Nuydens RM, Salmon PL, Meert TF (2004) Bone cancer pain model in mice: evaluation of pain behavior, bone destruction and morphine sensitivity. Pharmacol Biochem Be 79: 243-251. (Pubitemid 40029226)
33. Franchi S, Panerai AE, Sacerdote P (2007) Buprenorphine ameliorates the effect of surgery on hypothalamus-pituitary-adrenal axis, natural killer cell activity and metastatic colonization in rats in comparison with morphine or fentanyl treatment. Brain Behav Immun 21: 767-774. (Pubitemid 47002203)
34. Martucci C, Panerai AE, Sacerdote P (2004) Chronic fentanyl or buprenorphine infusion in the mouse: similar analgesic profile but different effects on immune responses. Pain 110: 385-392. (Pubitemid 38953304)
35. Valeberg BT, Rustoen T, Bjordal K, Hanestad BR, Paul S, et al. (2008) Self-reported prevalence, etiology, and characteristics of pain in oncology outpatients. Eur J Pain 12: 582-590.
36. van den Beuken-van Everdingen MHJ, de Rijke JM, Kessels AG, Schouten HC, van Kleef M, et al. (2007) Prevalence of pain in patients with cancer: a systematic review of the past 40 years. Ann Oncol 18: 1437-1449.
37. Medhurst S, Bowes M, Kidd BL, Glatt M, Muller M, et al. (2001) Antinociceptive effects of the bisphosphonate, zoledronic acid, in a novel rat model of bone cancer pain. Brit J Pharmacol 134.
38. Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology 153: 31-43. (Pubitemid 32127902)
39. Sufka KJ (1994) Conditioned place preference paradigm: a novel approach for analgesic drug assessment against chronic pain. Pain 58: 355-366.
40. Sufka KJ, Roach JT (1996) Stimulus properties and antinociceptive effects of selective bradykinin B1 and B2 receptor antagonists in rats. Pain 66: 99-103. (Pubitemid 26247029)
41. King T, Vera-Portocarrero L, Gutierrez T, Vanderah TW, Dussor G, et al. (2009) Unmasking the tonic-aversive state in neuropathic pain.[Erratum appears in Nat Neurosci. 2010 Aug;13(8):1033]. Nat Neurosci 12: 1364-1366.
42. Qu C, King T, Okun A, Lai J, Fields HL, et al. (2011) Lesion of the rostral anterior cingulate cortex eliminates the aversiveness of spontaneous neuropathic pain following partial or complete axotomy. Pain 152: 1641-1648.
43. Rutten K, De Vry J, Robens A, Tzschentke TM, van der Kam EL (2011) Dissociation of rewarding, anti-aversive and anti-nociceptive effects of different classes of anti-nociceptives in the rat. Eur J Pain 15: 299-305.
44. Davoody L, Quiton RL, Lucas JM, Ji Y, Keller A, et al. (2011) Conditioned place preference reveals tonic pain in an animal model of central pain. J Pain 12: 868-874.
45. Okun A, Liu P, Davis P, Ren J, Remeniuk B, et al. (2012) Afferent drive elicits ongoing pain in a model of advanced osteoarthritis. Pain 153: 924-933.
46. Park HJ, Stokes JA, Pirie E, Skahen J, Shtaerman Y, et al. (2013) Persistent hyperalgesia in the cisplatin-treated mouse as defined by threshold measures, the conditioned place preference paradigm, and changes in dorsal root ganglia activated transcription factor 3: the effects of gabapentin, ketorolac, and etanercept. Anesth Analg 116: 224-231.
47. Bateson PP, Rose SP, Horn G (1973) Imprinting: lasting effects on uracil incorporation into chick brain. Science 181: 576-578.
48. Bateson P (1991) Assessment of pain in animals. Anim Behav 42: 827-839.
49. McNabb CT, Uhelski ML, Fuchs PN (2012) A direct comparison of affective pain processing underlying two traditional pain modalities in rodents. Neurosci Lett 507: 57-61.
50. Urban R, Scherrer G, Goulding EH, Tecott LH, Basbaum AI (2011) Behavioral indices of ongoing pain are largely unchanged in male mice with tissue or nerve injury-induced mechanical hypersensitivity. Pain 152: 990-1000.
51. Hargreaves K, Dubner,R, Brown F, Flores C, Joris J (1988) Basic Section - A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32, 77-88.
52. Chin J, Kadhim S, Garcia B, Kim YS, Karlik S (1991) Magnetic resonance imaging for detecting and treatment monitoring of orthotopic murine bladder tumor implants. J Urology 145: 1297-1301.
53. Suzuki T, Tsuji M, Mori T, Misawa M, Endoh T, et al. (1996) Effect of the highly selective and nonpeptide delta opioid receptor agonist TAN-67 on the morphine-induced place preference in mice. J Pharmacol Exp Ther 279: 177-185. (Pubitemid 27166909)
54. Dashti-Rahmatababi MH, Hejazian SH, Morshedi A, Rafati A (2007) The analgesic effect of Carum copticum extract and morphine on phasic pain in mice. J Ethnopharmacol 109: 226-228. (Pubitemid 44959699)
55. Stevenson GW, Bilsky EJ, Negus SS (2006) Targeting pain-suppressed behaviours in preclinical assays of pain and analgesia: Effects of morphine on acetic acid-suppressed feeding in C57BL/6J mice. J Pain 7: 408-416. (Pubitemid 43794888)
56. Cesarovic N, Arras M, Jirkof P (2014) Impact of inhalation anaesthesia, surgery and analgesic treatment on home cage behaviour in laboratory mice. Appl Anim Behav Sci.
57. Hasegawa H, Saiki I (2002) Psychosocial stress augments tumor development through beta-adrenergic activation in mice. Jpn J Cancer Res 93: 729-735.
58. Betourne A, Familiades J, Lacassagne L, Halley H, Cazales M, et al. (2008) Decreased motivational properties of morphine in mouse models of cancerous- or inflammatory-chronic pain: implication of supraspinal neuropeptide FF2 receptors. Neuroscience 157: 12-21.
59. Matsumiya LC, Sorge RE, Sotocinal SG, Tabaka JM, Wieskopf JS, et al. (2012) Using the Mouse Grimace Scale to reevaluate the efficacy of postoperative analgesics in laboratory mice. J Am Assoc Lab Anim 51: 42-49.
60. Sasamura T, Nakamura S, Iida Y, Fujii H, Murata J, et al. (2002) Morphine analgesia suppresses tumor growth and metastasis in a mouse model of cancer pain produced by orthotopic tumor inoculation. Eur J Pharmacol 441: 185-191. (Pubitemid 34626170)
61. Liles JH, Flecknell PA (1993) The effects of surgical stimulus on the rat and the influence of analgesic treatment. Brit Vet J 149: 515-525. (Pubitemid 24010476)
62. Liles JH, Flecknell PA (1993) The influence of buprenorphine or bupivacaine on the post-operative effects of laparotomy and bile-duct ligation in rats. Lab Anim 27: 374-380. (Pubitemid 23304790)
63. Hayes JH, Flecknell PA (1999) A comparison of pre- and post-surgical administration of bupivacaine or buprenorphine following laparotomy in the rat. Lab Anim 33: 16-23. (Pubitemid 29050714)
64. Hayes KE, Raucci JA, Jr., Gades NM, Toth LA (2000) An evaluation of analgesic regimens for abdominal surgery in mice. Contemp Top Lab Anim 39: 18-23.
65. Roughan JV, Flecknell PA (2000) Effects of surgery and analgesic administration on spontaneous behaviour in singly housed rats. Res Vet Sci 69: 283-288. (Pubitemid 32109483)
66. Roughan JV, Flecknell RA (2004) Behaviour-based assessment of the duration of laparotomy-induced abdominal pain and the analgesic effects of carprofen and buprenorphine in rats. Behav Pharmacol 15: 461-472. (Pubitemid 39482935)
67. Craft RM, Henley SR, Haaseth RC, Hruby VJ, Porreca F (1995) Opioid antinociception in a rat model of visceral pain: systemic versus local drug administration. J Pharmacol Exp Ther 275: 1535-1542. (Pubitemid 26129945)
68. Nagahata S, Harano N, Ono K, Seta Y, Shiiba S, et al. (2007) A rat model for cancer pain in the trigemina nerve area. Eur J Pain 11: 69-69.
69. Dimitrijevic M, Laban O, Djuric VJ, Stanojevic S, Miletic T, et al. (2001) Behavior and Severity of Adjuvant Arthritis in Four Rat Strains. Brain Behav Immun 15: 255-265. (Pubitemid 33070958)
70. Kalueff AV, Tuohimaa P (2004) Grooming analysis algorithm for neurobehavioural stress research. Brain Res Protoc 13: 151-158. (Pubitemid 39030775)
71. Roughan JV, Flecknell PA, Davies BR (2004) Behavioural assessment of the effects of tumour growth in rats and the influence of the analgesics carprofen and meloxicam. Lab Anim 38: 286-296. (Pubitemid 38962078)
72. Mogil JS (2006) Sex, gender and pain. In: Cervero F, Jensen TS, editors. Handbook of Clinical Neurology. Amsterdam: Elsevier. 325-341.
73. Mogil JS (2012) Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon. Nat Rev Neurosci 13: 859-866.
74. Sorge RE, LaCroix-Fralish ML, Tuttle AH, Sotocinal SG, Austin J-S, et al. (2011) Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J Neurosci 31: 15450-15454.
75. Mogil JS, Chesler EJ, Wilson SG, Juraska JM, Sternberg WF (2000) Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype. Neurosci Biobehav R 24: 375-389. (Pubitemid 30227253)
76. Mogil JS, Wilson SG, Bon K, Lee SE, Kyungsoon C, et al. (1999) Heritaility of nociception I: Responses of 11 inbred mouse strains on 12 measures of nociception. Pain 80: 67-82. (Pubitemid 29151691)
77. Leach MC, Klaus K, Miller AL, Scotto di Perrotolo M, Sotocinal SG, et al. (2012) The assessment of post-vasectomy pain in mice using behaviour and the Mouse Grimace Scale. PLoS ONE [Electronic Resource] 7: e35656.
78. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, et al. (2010) Coding of facial expressions of pain in the laboratory mouse. Nat Methods 7: 447-449.
79. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. J Pharmacol Pharmacother 1: 94-99.