Improving the translation of analgesic drugs to the clinic: Animal models of neuropathic pain

British Journal of Pharmacology

Volumn 171, Issue 12, 2014, Pages 2951-2963

  Percie Du Sert, Nathalie ^a   Rice, A S C ^b,c  

^a National Centre for the Replacement   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c CHELSEA AND WESTMINSTER HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

analgesic; animal model; neuropathic pain; preclinical model; translation

Indexed keywords

ANALGESIC AGENT; CARBAMAZEPINE; DULOXETINE; GABAPENTIN;

ANIMAL BEHAVIOR; CHRONICITY; DISEASE MODEL; EXPERIMENTAL DESIGN; HUMAN; IN VIVO STUDY; INTERNAL VALIDITY; MEDICAL RESEARCH; METHODOLOGY; NEUROPATHIC PAIN; NONHUMAN; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; REVIEW; ANIMAL; NEURALGIA; PAIN MEASUREMENT; PATHOPHYSIOLOGY; REPRODUCIBILITY; SPECIES DIFFERENCE; TRANSLATIONAL RESEARCH;

ANALGESICS; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; NEURALGIA; PAIN MEASUREMENT; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84901419087     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12645     Document Type: Review

References (141)

1. Aicher SA, Silverman MB, Winkler CW, Bebo BF Jr, (2004). Hyperalgesia in an animal model of multiple sclerosis. Pain 110: 560-570.
2. Alabas OA, Tashani OA, Johnson MI, (2013). Effects of ethnicity and gender role expectations of pain on experimental pain: a cross-cultural study. Eur J Pain 17: 776-786.
3. Andersen ML, Tufik S, (2003). Sleep patterns over 21-day period in rats with chronic constriction of sciatic nerve. Brain Res 984: 84-92.
4. Andrews N, Harper S, Issop Y, Rice AS, (2011). Novel, nonreflex tests detect analgesic action in rodents at clinically relevant concentrations. Ann N Y Acad Sci 1245: 11-13.
5. Andrews N, Legg E, Lisak D, Issop Y, Richardson D, Harper S, et al. (2012). Spontaneous burrowing behaviour in the rat is reduced by peripheral nerve injury or inflammation associated pain. Eur J Pain 16: 485-495.
6. Attal N, Bouhassira D, Baron R, Dostrovsky J, Dworkin RH, Finnerup N, et al. (2011). Assessing symptom profiles in neuropathic pain clinical trials: can it improve outcome? Eur J Pain 15: 441-443.
7. Authier N, Gillet JP, Fialip J, Eschalier A, Coudore F, (2000). Description of a short-term Taxol-induced nociceptive neuropathy in rats. Brain Res 887: 239-249.
8. Authier N, Gillet JP, Fialip J, Eschalier A, Coudore F, (2003a). An animal model of nociceptive peripheral neuropathy following repeated cisplatin injections. Exp Neurol 182: 12-20.
9. Authier N, Gillet JP, Fialip J, Eschalier A, Coudore F, (2003b). A new animal model of vincristine-induced nociceptive peripheral neuropathy. Neurotoxicology 24: 797-805.
10. Authier N, Balayssac D, Marchand F, Ling B, Zangarelli A, Descoeur J, et al. (2009). Animal models of chemotherapy-evoked painful peripheral neuropathies. Neurotherapeutics 6: 620-629.
11. Babcock DT, Shi S, Jo J, Shaw M, Gutstein HB, Galko MJ, (2011). Hedgehog signaling regulates nociceptive sensitization. Curr Biol 21: 1525-1533.
12. Backonja M, Beydoun A, Edwards KR, Schwartz SL, Fonseca V, Hes M, et al. (1998). Gabapentin for the symptomatic treatment of painful neuropathy in patients with diabetes mellitus: a randomized controlled trial. JAMA 280: 1831-1836.
13. Backonja MM, Stacey B, (2004). Neuropathic pain symptoms relative to overall pain rating. J Pain 5: 491-497.
14. Barnett SA, (2009) The Rat: A Study in Behaviour. Aldine Transaction: London.
15. Barnett SA, Whishaw IQ, Kolb B, (2006) The Behaviour of the Laboratory Rat. 1. Oxford University Press: Oxford.
16. Baron R, Binder A, Wasner G, (2010). Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment. Lancet Neurol 9: 807-819.
17. Bebarta V, Luyten D, Heard K, (2003). Emergency medicine animal research: does use of randomization and blinding affect the results? Acad Emerg Med 10: 684-687.
18. Benbouzid M, Pallage V, Rajalu M, Waltisperger E, Doridot S, Poisbeau P, et al. (2008). Sciatic nerve cuffing in mice: a model of sustained neuropathic pain. Eur J Pain 12: 591-599.
19. Berge OG, (2011). Predictive validity of behavioural animal models for chronic pain. Br J Pharmacol 164: 1195-1206.
20. Blackburn-Munro G, (2004). Pain-like behaviours in animals-how human are they? Trends Pharmacol Sci 25: 299-305.
21. Borsook D, Becerra LR, (2006). Breaking down the barriers: fMRI applications in pain, analgesia and analgesics. Mol Pain 2: 30.
22. Bouhassira D, Lanteri-Minet M, Attal N, Laurent B, Touboul C, (2008). Prevalence of chronic pain with neuropathic characteristics in the general population. Pain 136: 380-387.
23. Brown DC, Boston R, Coyne JC, Farrar JT, (2009). A novel approach to the use of animals in studies of pain: validation of the canine brief pain inventory in canine bone cancer. Pain Med 10: 133-142.
24. Burgess G, Williams D, (2010). The discovery and development of analgesics: new mechanisms, new modalities. J Clin Invest 120: 3753-3759.
25. Campbell CM, Kipnes MS, Stouch BC, Brady KL, Kelly M, Schmidt WK, et al. (2012). Randomized control trial of topical clonidine for treatment of painful diabetic neuropathy. Pain 153: 1815-1823.
26. Cao L, Butler MB, Tan L, Draleau KS, Koh WY, (2012). Murine immunodeficiency virus-induced peripheral neuropathy and the associated cytokine responses. J Immunol 189: 3724-3733.
27. Clements DN, Carter SD, Innes JF, Ollier WE, Day PJ, (2006). Analysis of normal and osteoarthritic canine cartilage mRNA expression by quantitative polymerase chain reaction. Arthritis Res Ther 8: R158.
28. Cobos EJ, Ghasemlou N, Araldi D, Segal D, Duong K, Woolf CJ, (2012). Inflammation-induced decrease in voluntary wheel running in mice: a nonreflexive test for evaluating inflammatory pain and analgesia. Pain 153: 876-884.
29. Craig AD, (2009). A rat is not a monkey is not a human: comment on Mogil (Nature Rev. Neurosci. 10, 283-294 (2009)). Nat Rev Neurosci 10: 466.
30. Currie GL, Delaney A, Bennett M, Dickenson AH, Egan K, Vesterinen HM, et al. (2013). Animal models of bone cancer pain: systematic review and meta-analyses. Pain 154: 917-926.
31. Dahan A, Kest B, Waxman AR, Sarton E, (2008). Sex-specific responses to opiates: animal and human studies. Anesth Analg 107: 83-95.
32. D'Almeida JA, de Castro-Costa CM, Frota CH, Severo JF, Rocha TD, Nogueira TF, (1999). Behavioral changes of Wistar rats with experimentally-induced painful diabetic neuropathy. Arq Neuropsiquiatr 57 (3B): 746-752.
33. Deacon RM, (2006). Burrowing in rodents: a sensitive method for detecting behavioral dysfunction. Nat Protoc 1: 118-121.
34. Deacon RM, (2009). Burrowing: a sensitive behavioural assay, tested in five species of laboratory rodents. Behav Brain Res 200: 128-133.
35. Deacon RM, Reisel D, Perry VH, Nicholas J, Rawlins P, (2005). Hippocampal scrapie infection impairs operant DRL performance in mice. Behav Brain Res 157: 99-105.
36. Dworkin RH, O'Connor AB, Backonja M, Farrar JT, Finnerup NB, Jensen TS, et al. (2007). Pharmacologic management of neuropathic pain: evidence-based recommendations. Pain 132: 237-251.
37. Dworkin RH, Turk DC, Wyrwich KW, Beaton D, Cleeland CS, Farrar JT, et al. (2008). Interpreting the clinical importance of treatment outcomes in chronic pain clinical trials: IMMPACT recommendations. J Pain 9: 105-121.
38. Dworkin RH, O'Connor AB, Audette J, Baron R, Gourlay GK, Haanpaa ML, et al. (2010a). Recommendations for the pharmacological management of neuropathic pain: an overview and literature update. Mayo Clin Proc 85 (3 Suppl.): S3-S14.
39. Dworkin RH, Turk DC, Peirce-Sandner S, McDermott MP, Farrar JT, Hertz S, et al. (2010b). Placebo and treatment group responses in postherpetic neuralgia versus painful diabetic peripheral neuropathy clinical trials in the REPORT database. Pain 150: 12-16.
40. Dworkin RH, Turk DC, Peirce-Sandner S, He H, McDermott MP, Farrar JT, et al. (2013). Assay sensitivity and study features in neuropathic pain trials: an ACTTION meta-analysis. Neurology 81: 67-75.
41. EFPIA (2013). The pharmaceutical industry in figures. Available at: http://www.efpia.eu/uploads/Figures-Key-Data-2013.pdf (accessed 1/10/2013).
42. Eisenach JC, Lindner MD, (2004). Did experimenter bias conceal the efficacy of spinal opioids in previous studies with the spinal nerve ligation model of neuropathic pain? Anesthesiology 100: 765-767.
43. FDA (2011). Is it true FDA is approving fewer new drugs lately ? Available at: http://www.fda.gov/downloads/AboutFDA/Transparency/Basics/ UCM247465.pdf (accessed 21/1/2013).
44. FDA (2012). Novel new drugs 2011. Available at: http://www.fda.gov/ downloads/Drugs/DevelopmentApprovalProcess/DrugInnovation/ucm293663.pdf (accessed 21/1/2013).
45. Field MJ, Oles RJ, Lewis AS, McCleary S, Hughes J, Singh L, (1997). Gabapentin (neurontin) and S-(+)-3-isobutylgaba represent a novel class of selective antihyperalgesic agents. Br J Pharmacol 121: 1513-1522.
46. Finnerup NB, Otto M, McQuay HJ, Jensen TS, Sindrup SH, (2005). Algorithm for neuropathic pain treatment: an evidence based proposal. Pain 118: 289-305.
47. Finnerup NB, Sindrup SH, Jensen TS, (2010). The evidence for pharmacological treatment of neuropathic pain. Pain 150: 573-581.
48. Flatters SJ, Bennett GJ, (2004). Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain 109: 150-161.
49. Fleetwood-Walker SM, Quinn JP, Wallace C, Blackburn-Munro G, Kelly BG, Fiskerstrand CE, et al. (1999). Behavioural changes in the rat following infection with varicella-zoster virus. J Gen Virol 80 (Pt 9): 2433-2436.
50. Freeman R, Baron R, Bouhassira D, Cabrera J, Emir B, (2014). Sensory profiles of patients with neuropathic pain based on the neuropathic pain symptoms and signs. Pain 155: 367-376.
51. Garry EM, Delaney A, Anderson HA, Sirinathsinghji EC, Clapp RH, Martin WJ, et al. (2005). Varicella zoster virus induces neuropathic changes in rat dorsal root ganglia and behavioral reflex sensitisation that is attenuated by gabapentin or sodium channel blocking drugs. Pain 118: 97-111.
52. Gonzalez-Nunez V, Rodriguez RE, (2009). The zebrafish: a model to study the endogenous mechanisms of pain. ILAR J 50: 373-386.
53. Hahm TS, Ahn HJ, Ryu S, Gwak MS, Choi SJ, Kim JK, et al. (2012). Combined carbamazepine and pregabalin therapy in a rat model of neuropathic pain. Br J Anaesth 109: 968-974.
54. Hasnie FS, Breuer J, Parker S, Wallace V, Blackbeard J, Lever I, et al. (2007). Further characterization of a rat model of varicella zoster virus-associated pain: relationship between mechanical hypersensitivity and anxiety-related behavior, and the influence of analgesic drugs. Neuroscience 144: 1495-1508.
55. Hole K, Tjolsen A, (1993). The tail-flick and formalin tests in rodents: changes in skin temperature as a confounding factor. Pain 53: 247-254.
56. Hu B, Doods H, Treede RD, Ceci A, (2009). Depression-like behaviour in rats with mononeuropathy is reduced by the CB2-selective agonist GW405833. Pain 143: 206-212.
57. Huang W, Calvo M, Karu K, Olausen H, Bathgate G, Okuse K, et al. (2013). A clinically relevant rodent model of HIV antiretroviral drug stavudine induced painful peripheral neuropathy. Pain 154: 560-575.
58. Jensen TS, Baron R, Haanpaa M, Kalso E, Loeser JD, Rice AS, et al. (2011). A new definition of neuropathic pain. Pain 152: 2204-2205.
59. Jirkof P, Cesarovic N, Rettich A, Nicholls F, Seifert B, Arras M, (2010). Burrowing behavior as an indicator of post-laparotomy pain in mice. Front Behav Neurosci 4: 165.
60. Joseph EK, Chen X, Khasar SG, Levine JD, (2004). Novel mechanism of enhanced nociception in a model of AIDS therapy-induced painful peripheral neuropathy in the rat. Pain 107: 147-158.
61. Keating SC, Thomas AA, Flecknell PA, Leach MC, (2012). Evaluation of EMLA cream for preventing pain during tattooing of rabbits: changes in physiological, behavioural and facial expression responses. PLoS ONE 7: e44437.
62. Khanna I, (2012). Drug discovery in pharmaceutical industry: productivity challenges and trends. Drug Discov Today 17: 1088-1102.
63. Kilkenny C, Parsons N, Kadyszewski E, Festing MF, Cuthill IC, Fry D, et al. (2009). Survey of the quality of experimental design, statistical analysis and reporting of research using animals. PLoS ONE 4: e7824.
64. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010a). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
65. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG, (2010b). Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412.
66. King T, Vera-Portocarrero L, Gutierrez T, Vanderah TW, Dussor G, Lai J, et al. (2009). Unmasking the tonic-aversive state in neuropathic pain. Nat Neurosci 12: 1364-1366.
67. Kissin I, (2010). The development of new analgesics over the past 50 years: a lack of real breakthrough drugs. Anesth Analg 110: 780-789.
68. Kola I, Landis J, (2004). Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov 3: 711-715.
69. Kontinen VK, Meert TF, (2003) Predictive validity of neuropathic pain models in pharmacological studies with behavioural outcome in the rat: a systematic review. In:, Dostrovsky JO, Carr DB, Koltzenburg M, (eds). Proceedings of the 10th World Congress on Pain. IASP Press: Seattle, pp. 489-498.
70. Kontinen VK, Kauppila T, Paananen S, Pertovaara A, Kalso E, (1999). Behavioural measures of depression and anxiety in rats with spinal nerve ligation-induced neuropathy. Pain 80: 341-346.
71. Laast VA, Shim B, Johanek LM, Dorsey JL, Hauer PE, Tarwater PM, et al. (2011). Macrophage-mediated dorsal root ganglion damage precedes altered nerve conduction in SIV-infected macaques. Am J Pathol 179: 2337-2345.
72. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, et al. (2006). Social modulation of pain as evidence for empathy in mice. Science 312: 1967-1970.
73. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, et al. (2010). Coding of facial expressions of pain in the laboratory mouse. Nat Methods 7: 447-449.
74. Lascelles BD, DePuy V, Thomson A, Hansen B, Marcellin-Little DJ, Biourge V, et al. (2010). Evaluation of a therapeutic diet for feline degenerative joint disease. J Vet Intern Med 24: 487-495.
75. Lascelles BDX, Flecknell PA, (2010). Do animal models tell us about human pain? Pain Clin Updates 18: 1-6.
76. Leach MC, Klaus K, Miller AL, Scotto di Perrotolo M, Sotocinal SG, Flecknell PA, (2012). The assessment of post-vasectomy pain in mice using behaviour and the Mouse Grimace Scale. PLoS ONE 7: e35656.
77. Ling B, Authier N, Balayssac D, Eschalier A, Coudore F, (2007). Behavioral and pharmacological description of oxaliplatin-induced painful neuropathy in rat. Pain 128: 225-234.
78. Lisi L, Navarra P, Cirocchi R, Sharp A, Stigliano E, Feinstein DL, et al. (2012). Rapamycin reduces clinical signs and neuropathic pain in a chronic model of experimental autoimmune encephalomyelitis. J Neuroimmunol 243: 43-51.
79. Macleod MR, van der Worp HB, Sena ES, Howells DW, Dirnagl U, Donnan GA, (2008). Evidence for the efficacy of NXY-059 in experimental focal cerebral ischaemia is confounded by study quality. Stroke 39: 2824-2829.
80. Macleod MR, Fisher M, O'Collins V, Sena ES, Dirnagl U, Bath PM, et al. (2009). Good laboratory practice: preventing introduction of bias at the bench. Stroke 40: e50-e52.
81. Maier C, Baron R, Tolle TR, Binder A, Birbaumer N, Birklein F, et al. (2010). Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): somatosensory abnormalities in 1236 patients with different neuropathic pain syndromes. Pain 150: 439-450.
82. Malcangio M, Tomlinson DR, (1998). A pharmacologic analysis of mechanical hyperalgesia in streptozotocin/diabetic rats. Pain 76: 151-157.
83. Matson DJ, Broom DC, Carson SR, Baldassari J, Kehne J, Cortright DN, (2007). Inflammation-induced reduction of spontaneous activity by adjuvant: a novel model to study the effect of analgesics in rats. J Pharmacol Exp Ther 320: 194-201.
84. Matsumiya LC, Sorge RE, Sotocinal SG, Tabaka JM, Wieskopf JS, Zaloum A, et al. (2012). Using the Mouse Grimace Scale to reevaluate the efficacy of postoperative analgesics in laboratory mice. J Am Assoc Lab Anim Sci 51: 42-49.
85. Matthies BK, Franklin KB, (1992). Formalin pain is expressed in decerebrate rats but not attenuated by morphine. Pain 51: 199-206.
86. Merksey H, Bogduk N, (1994) Classification of Chronic Pain, 2nd edn. IASP Press: Seattle.
87. Milinkeviciute G, Gentile C, Neely GG, (2012). Drosophila as a tool for studying the conserved genetics of pain. Clin Genet 82: 359-366.
88. Mizisin AP, Shelton GD, Burgers ML, Powell HC, Cuddon PA, (2002). Neurological complications associated with spontaneously occurring feline diabetes mellitus. J Neuropathol Exp Neurol 61: 872-884.
89. Mogil JS, (2009). Animal models of pain: progress and challenges. Nat Rev Neurosci 10: 283-294.
90. Mogil JS, (2012). Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon. Nat Rev Neurosci 13: 859-866.
91. Mogil JS, Crager SE, (2004). What should we be measuring in behavioral studies of chronic pain in animals? Pain 112: 12-15.
92. Mogil JS, Miermeister F, Seifert F, Strasburg K, Zimmermann K, Reinold H, et al. (2005). Variable sensitivity to noxious heat is mediated by differential expression of the CGRP gene. Proc Natl Acad Sci U S A 102: 12938-12943.
93. Mogil JS, Davis KD, Derbyshire SW, (2010a). The necessity of animal models in pain research. Pain 151: 12-17.
94. Mogil JS, Graham AC, Ritchie J, Hughes SF, Austin JS, Schorscher-Petcu A, et al. (2010b). Hypolocomotion, asymmetrically directed behaviors (licking, lifting, flinching, and shaking) and dynamic weight bearing (gait) changes are not measures of neuropathic pain in mice. Mol Pain 6: 34.
95. Moore A, Derry S, Eccleston C, Kalso E, (2013). Expect analgesic failure; pursue analgesic success. BMJ 346: f2690.
96. Morimoto S, Ito M, Oda S, Sugiyama A, Kuroda M, Adachi-Akahane S, (2012). Spinal mechanism underlying the antiallodynic effect of gabapentin studied in the mouse spinal nerve ligation model. J Pharmacol Sci 118: 455-466.
97. Muhlhausler BS, Bloomfield FH, Gillman MW, (2013). Whole animal experiments should be more like human randomized controlled trials. PLoS Biol 11: e1001481.
98. Munos B, (2009). Lessons from 60 years of pharmaceutical innovation. Nat Rev Drug Discov 8: 959-968.
99. Neely GG, Kuba K, Cammarato A, Isobe K, Amann S, Zhang L, et al. (2010). A global in vivo Drosophila RNAi screen identifies NOT3 as a conserved regulator of heart function. Cell 141: 142-153.
100. Niesters M, Dahan A, Kest B, Zacny J, Stijnen T, Aarts L, et al. (2010). Do sex differences exist in opioid analgesia? A systematic review and meta-analysis of human experimental and clinical studies. Pain 151: 61-68.
101. Olmarker K, Storkson R, Berge OG, (2002). Pathogenesis of sciatic pain: a study of spontaneous behavior in rats exposed to experimental disc herniation. Spine (Phila Pa 1976) 27: 1312-1317.
102. Phillips TJ, Cherry CL, Cox S, Marshall SJ, Rice AS, (2010). Pharmacological treatment of painful HIV-associated sensory neuropathy: a systematic review and meta-analysis of randomised controlled trials. PLoS ONE 5: e14433.
103. Pickering G, Jourdan D, Millecamps M, Chapuy E, Alliot J, Eschalier A, (2006). Age-related impact of neuropathic pain on animal behaviour. Eur J Pain 10: 749-755.
104. Polomano RC, Mannes AJ, Clark US, Bennett GJ, (2001). A painful peripheral neuropathy in the rat produced by the chemotherapeutic drug, paclitaxel. Pain 94: 293-304.
105. Quessy SN, (2009). Comment on: animal models and the prediction of efficacy in clinical trials of analgesic drugs: a critical appraisal and a call for uniform reporting standards. Pain 142: 284-285.
106. Rice AS, (2010) Predicting analgesic efficacy from animal models of peripheral neuropathy and nerve injury: a critical view from the clinic. In:, Mogil JS, (ed.). Pain 2010-An Updated Review: Refresher Course Syllabus. IASP Press: Seattle, pp. 415-426.
107. Rice AS, Maton S, (2001). Gabapentin in postherpetic neuralgia: a randomised, double blind, placebo controlled study. Pain 94: 215-224.
108. Rice AS, Cimino-Brown D, Eisenach JC, Kontinen VK, Lacroix-Fralish ML, Machin I, et al. (2009). Animal models and the prediction of efficacy in clinical trials of analgesic drugs: a critical appraisal and call for uniform reporting standards. Pain 139: 243-247.
109. Rice AS, Morland R, Huang W, Currie GL, Sena ES, Macleod M, (2013). Transparency in the reporting of in vivo preclinical pain research: the relevance and implications of the ARRIVE (Animal Research: Reporting In Vivo Experiments) guidelines. Scand J Pain 4: 58-62.
110. Robinson I, Dowdall T, Meert TF, (2004). Development of neuropathic pain is affected by bedding texture in two models of peripheral nerve injury in rats. Neurosci Lett 368: 107-111.
111. Roeska K, Ceci A, Treede RD, Doods H, (2009a). Effect of high trait anxiety on mechanical hypersensitivity in male rats. Neurosci Lett 464: 160-164.
112. Roeska K, Doods H, Arndt K, Treede RD, Ceci A, (2009b). Anxiety-like behaviour in rats with mononeuropathy is reduced by the analgesic drugs morphine and gabapentin. Pain 139: 349-357.
113. Rooke ED, Vesterinen HM, Sena ES, Egan KJ, Macleod MR, (2011). Dopamine agonists in animal models of Parkinson's disease: a systematic review and meta-analysis. Parkinsonism Relat Disord 17: 313-320.
114. Rowbotham M, Harden N, Stacey B, Bernstein P, Magnus-Miller L, (1998). Gabapentin for the treatment of postherpetic neuralgia: a randomized controlled trial. JAMA 280: 1837-1842.
115. Rowbotham MC, (2009). The case for publishing 'negative' clinical trials. Pain 146: 225-226.
116. Salinas FA, Lugo LH, Garcia HI, (2012). Efficacy of early treatment with carbamazepine in prevention of neuropathic pain in patients with spinal cord injury. Am J Phys Med Rehabil 91: 1020-1027.
117. Schreiber AK, Neufeld M, Jesus CH, Cunha JM, (2012). Peripheral antinociceptive effect of anandamide and drugs that affect the endocannabinoid system on the formalin test in normal and streptozotocin-diabetic rats. Neuropharmacology 63: 1286-1297.
118. Sena ES, van der Worp HB, Bath PM, Howells DW, Macleod MR, (2010). Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol 8: e1000344.
119. Serra J, (2012). Microneurography: towards a biomarker of spontaneous pain. Pain 153: 1989-1990.
120. Sneddon LU, (2004). Evolution of nociception in vertebrates: comparative analysis of lower vertebrates. Brain Res Brain Res Rev 46: 123-130.
121. Sneddon LU, (2009). Pain perception in fish: indicators and endpoints. ILAR J 50: 338-342.
122. Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS, et al. (2011). The Rat Grimace Scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions. Mol Pain 7: 55.
123. Sun W, Miao B, Wang XC, Duan JH, Ye X, Han WJ, et al. (2012). Gastrodin inhibits allodynia and hyperalgesia in painful diabetic neuropathy rats by decreasing excitability of nociceptive primary sensory neurons. PLoS ONE 7: e39647.
124. Tesch GH, Allen TJ, (2007). Rodent models of streptozotocin-induced diabetic nephropathy. Nephrology (Carlton) 12: 261-266.
125. Torrance N, Smith BH, Bennett MI, Lee AJ, (2006). The epidemiology of chronic pain of predominantly neuropathic origin. Results from a general population survey. J Pain 7: 281-289.
126. Treede RD, Jensen TS, Campbell JN, Cruccu G, Dostrovsky JO, Griffin JW, et al. (2008). Neuropathic pain: redefinition and a grading system for clinical and research purposes. Neurology 70: 1630-1635.
127. Tsilidis KK, Panagiotou OA, Sena ES, Aretouli E, Evangelou E, Howells DW, et al. (2013). Evaluation of excess significance bias in animal studies of neurological diseases. PLoS Biol 11: e1001609.
128. Vasconcelos M, Hollis K, Nowbahari E, Kacelnik A, (2012). Pro-sociality without empathy. Biol Lett 8: 910-912.
129. Vesterinen HM, Sena ES, ffrench-Constant C, Williams A, Chandran S, Macleod MR, (2010). Improving the translational hit of experimental treatments in multiple sclerosis. Mult Scler 16: 1044-1055.
130. Vierck CJ, Mauderli AP, Wiley RG, (2005). Assessment of pain in laboratory animals: a comment on Mogil and Crager (2004). Pain 114: 520-523, author reply 523-524.
131. Vierck CJ, Hansson PT, Yezierski RP, (2008). Clinical and pre-clinical pain assessment: are we measuring the same thing? Pain 135: 7-10.
132. Wallace VC, Blackbeard J, Pheby T, Segerdahl AR, Davies M, Hasnie F, et al. (2007a). Pharmacological, behavioural and mechanistic analysis of HIV-1 gp120 induced painful neuropathy. Pain 133: 47-63.
133. Wallace VC, Blackbeard J, Segerdahl AR, Hasnie F, Pheby T, McMahon SB, et al. (2007b). Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain. Brain 130 (Pt 10): 2688-2702.
134. Wallace VC, Segerdahl AR, Lambert DM, Vandevoorde S, Blackbeard J, Pheby T, et al. (2007c). The effect of the palmitoylethanolamide analogue, palmitoylallylamide (L-29) on pain behaviour in rodent models of neuropathy. Br J Pharmacol 151: 1117-1128.
135. Wallace VC, Segerdahl AR, Blackbeard J, Pheby T, Rice AS, (2008). Anxiety-like behaviour is attenuated by gabapentin, morphine and diazepam in a rodent model of HIV anti-retroviral-associated neuropathic pain. Neurosci Lett 448: 153-156.
136. Wasserman JK, Koeberle PD, (2009). Development and characterization of a hemorrhagic rat model of central post-stroke pain. Neuroscience 161: 173-183.
137. Wernham BG, Trumpatori B, Hash J, Lipsett J, Davidson G, Wackerow P, et al. (2011). Dose reduction of meloxicam in dogs with osteoarthritis-associated pain and impaired mobility. J Vet Intern Med 25: 1298-1305.
138. Whiteside GT, Adedoyin A, Leventhal L, (2008). Predictive validity of animal pain models? A comparison of the pharmacokinetic-pharmacodynamic relationship for pain drugs in rats and humans. Neuropharmacology 54: 767-775.
139. Wiffen PJ, Derry S, Moore RA, Aldington D, Cole P, Rice AS, et al. (2013). Antiepileptic drugs for neuropathic pain and fibromyalgia-an overview of Cochrane reviews. Cochrane Database Syst Rev (11): CD010567.
140. Yoshizumi M, Parker RA, Eisenach JC, Hayashida K, (2012). Gabapentin inhibits gamma-amino butyric acid release in the locus coeruleus but not in the spinal dorsal horn after peripheral nerve injury in rats. Anesthesiology 116: 1347-1353.
141. Zheng FY, Xiao WH, Bennett GJ, (2011). The response of spinal microglia to chemotherapy-evoked painful peripheral neuropathies is distinct from that evoked by traumatic nerve injuries. Neuroscience 176: 447-454.