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Animal Models of Pain: Progress and Challenges

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Animal Models of Pain: Progress and Challenges REVIEWS Animal models of pain: progress and challenges Jeffrey S. Mogil Abstract | Many are frustrated with the lack of translational progress in the pain field, in which huge gains in basic science knowledge obtained using animal models have not led to the development of many new clinically effective compounds. A careful re-examination of animal models of pain is therefore warranted. Pain researchers now have at their disposal a much wider range of mutant animals to study, assays that more closely resemble clinical pain states, and dependent measures beyond simple reflexive withdrawal. However, the complexity of the phenomenon of pain has made it difficult to assess the true value of these advances. In addition, pain studies are importantly affected by a wide range of modulatory factors, including sex, genotype and social communication, all of which must be taken into account when using an animal model. Therapeutic index Pain is both a highly important health problem and an The debate is complicated by the lack of published The ratio of the minimum dose increasingly mature topic of study. Experiments on pain negative data, both from animal studies and from clini- of a drug that causes toxic using human subjects are practically challenging, funda- cal trials. However, in general animal models are thought effects to the therapeutic dose, mentally (and perhaps inescapably) subjective, and ethi- to be fairly effective in ‘backward’ validation (detecting used as a relative measure of cally self-limiting, and thus laboratory animal models analgesic activity of drugs already known to be clini- drug safety. of pain are widely used (BOX 1). However, pain studies cally effective)7,8, but less so in the forward validation Neuropathic pain using non-human animals pose their own significant required for the drug development process. It should be Pain arising as a direct challenges and ethical constraints. Moreover, a vigor- noted that the blame for a failed clinical trial should not consequence of a lesion or ous debate as to the value of currently popular animal automatically be shouldered by the animal model; poor disease affecting the somatosensory system. models has emerged among pain researchers. clinical-trial design or implementation and the lack of Frustration is mounting over the limited success of the sufficiently sensitive toxicity screens for important side Reflexive measures field in translating the veritable explosion of basic scien- effects may also play their part. Excellent discussions of Measures of involuntary tific data collected over the past few decades using animal the predictive validity of animal models of neuropathic movements made in response models into truly new, effective and safe clinical analge- pain can be found in recent reviews7–10. to a stimulus. For example, the nociceptive withdrawal reflex is sics. Failures have been related to both adverse side effects Assuming that current animal models of pain are a spinal (segmental) reflex and lack of efficacy in humans of drugs that seemed to suboptimal, proposals for improvement can be grouped intended to protect the body be safe and effective in animal models. Although pain into several categories: refinement of current models to from potentially damaging is by no means alone in having an uninspiring transla- improve their accuracy and reduce their variability 11, noxious stimuli. 1 Spino-bulbospinal reflexes, lost tion record , some have called for the abandonment of development of new models more directly applicable after spinal transection but animal pain studies in favour of more extensive testing of to prevalent painful conditions or more accurately able to preserved after decerebration, humans2. Notably, the field has endured one very high pro- predict the outcome measures used in clinical trials, include licking, guarding, file efficacy-related failure in neurokinin 1 (substance P) replacement of reflexive measures with non-reflexive (operant) vocalizing and jumping. receptor antagonists3, and less discussed failures such as measures12, replacement of measurements of evoked 4 + 5 Department of Psychology glycine-site antagonists and Na channel blockers . By responses with measurements of spontaneous behav- 13 and Alan Edwards Centre for contrast, the synthetic ω-conotoxin ziconotide (Prialt) iours , and the use of a broader range of ‘quality of life’ Research on Pain, McGill provides an example of a ‘rationally designed’ analgesic6, measures14. University, Montreal, Quebec the efficacy of which in humans was correctly predicted The present Review endeavours to describe the nature H3A 1B1, Canada. by animal models. However, ziconotide is hardly an and implementation of behavioural animal models of pain, e-mail: [email protected] unqualified success story: its intrathecal route of admin- with an emphasis on their complexities and limitations and doi:10.1038/nrn2606 istration and narrow therapeutic index have prevented it on strategies for improvement. The stakes are enormous, Published online 4 March 2009 from being widely adopted clinically. given the impact of pain (which costs US$1 trillion per NATURE REVIEWS | NEUROSCIENCE VOLUME 10 | APRIL 2009 | 283 )''0DXZd`ccXeGlYc`j_\ijC`d`k\[%8cci`^_kji\j\im\[ REVIEWS 15 16 Non-reflexive (operant) year in developed countries ) on society and the central both experimental and clinical pain . Nonetheless, the measures role of animal models in analgesic drug development and subjectivity of these measures has led to a decades-long Measures of behaviours that the basic science that drives it. I discuss topics related search for surrogate biomarkers. To date, no objective require spinal-cerebrospinal to the choice of subjects (and modulatory factors), assays surrogate with acceptably high sensitivity and specificity integration, which are lost after decerebration. The use of and finally measures in pain studies using animals. has been found and independently replicated. Individual operant measures specifically functional-imaging scans may one day provide a reliable requires a learned, motivated Behaving animals as the subjects of pain studies and objective measurement of the subjective percep- behaviour that terminates Why do we need animal models? Human self-ratings tion of pain17, but that day has not yet arrived. Genetic exposure to the noxious of pain, using both questionnaires and scales, are reli- biomarkers are another theoretical option; however, it is stimulus. able, accurate and versatile for the measurement of likely that too many genes are involved18 for any genetic ‘pain fingerprint’ to be developed in the foreseeable future. Even if this were achieved, genomic DNA vari- Box 1 | What exactly is an animal ‘model’? ants would predict trait sensitivity to pain rather than ongoing levels of pain. Subject Assay Measure Non-human animals cannot self-report, but their Species Etiology Reflex behaviours in response to noxious stimuli can be reli- + . Nociceptive . Heat or cold (thermal, mechanical, . Mechanical ably and objectively scored. However, the most reliable Strain chemical or electrical) + and commonly scored behaviours are simple reflexes + . Inflammatory Spontaneous or innate responses (such as licking an inflamed paw), (algogen, sensitizing . Autotomy which seem to lack clinical face validity. Some basic pain Mutant? compound, inflammatory . Directed behaviours researchers have opted to use proxy models — in which + mediator, polyarthritic (biting, flinching, guarding, or monoarthritic) licking, lifting and shaking) animals are either anaesthetized or in vitro or ex vivo Sex . Neuropathic . Gait or posture preparations are used. Techniques used include cell cul- + (surgical or chemical) + ture, the measurement of immediate-early gene expres- Age . Disease state Operant sion or neuronal firing, and small-animal imaging. In (e.g. cancer, complex + . Learned escape some cases these proxies can be combined with behav- regional pain syndrome 1) . Place aversion Husbandry + . Reinforcement conflict ioural measures; for example, under light anaesthesia . Cage density + electrophysiological recordings and observation of reflex- . Diet Body part . Cutaneous Pain-affected complex ive withdrawals from noxious stimuli can be performed . Social factors 19 . Muscular behaviours simultaneously . Much important information has been + .Orofacial . Anxiety learned from these models. Furthermore, one could Testing procedures . Visceral . Attention . Disability argue that behavioural measures are themselves proxies . Arousal + . Communication . Sociability of a subjective perception to which the experimenter has . Handling Time point . Sleep no direct access. However, with awake, behaving animals no . Restraint post-injury assumptions regarding anatomy and pathophysiology When animal models of pain are discussed, confusion can result from the use of the single need to be made. Therefore the dominant paradigm word ‘model’ to refer to three entirely separate entities: the subject, the assay and the in basic science and analgesic drug development is to Nature Reviews | Neuroscience measure (see the figure). Some use the word model to refer to the experimental subject, use behavioural pharmacology in laboratory animals. such as a transgenic mutant, or a species or strain that is sensitive (or resistant) to pain or Indeed, experiments featuring behavioural measure- that spontaneously develops a painful disease. When selecting a subject, other ments of pain in animals are becoming more common considerations include
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