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Opportunities for Improving Animal Welfare in Rodent Models of Epilepsy and Seizures

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Opportunities for Improving Animal Welfare in Rodent Models of Epilepsy and Seizures Accepted Manuscript Title: Opportunities for improving animal welfare in rodent models of epilepsy and seizures Author: Katie Lidster John G. Jefferys Ingmar Blumcke¨ Vincenzo Crunelli Paul Flecknell Bruno G. Frenguelli William P. Gray Rafal Kaminski Asla Pitkanen¨ Ian Ragan Mala Shah Michele Simonato Andrew Trevelyan Holger Volk Matthew Walker Neil Yates Mark J. Prescott PII: S0165-0270(15)00340-4 DOI: http://dx.doi.org/doi:10.1016/j.jneumeth.2015.09.007 Reference: NSM 7336 To appear in: Journal of Neuroscience Methods Received date: 9-7-2015 Revised date: 1-9-2015 Accepted date: 8-9-2015 Please cite this article as: Lidster K, Jefferys JG, Blumcke¨ I, Crunelli V, Flecknell P, Frenguelli BG, Gray WP, Kaminski R, Pitkanen¨ A, Ragan I, Shah M, Simonato M, Trevelyan A, Volk H, Walker M, Yates N, Prescott MJ, Opportunities for improving animal welfare in rodent models of epilepsy and seizures, Journal of Neuroscience Methods (2015), http://dx.doi.org/10.1016/j.jneumeth.2015.09.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Lidster et al. 1 Opportunities for improving animal welfare in rodent models of epilepsy and seizures 1 Katie Lidster* 1, John G. Jefferys 2, Ingmar Blümcke 3, Vincenzo Crunelli 4, Paul Flecknell 5, Bruno G. Frenguelli 6, William P. Gray 7, Rafal Kaminski 8, Asla Pitkänen 9, Ian Ragan 10 , Mala Shah 11 , Michele Simonato 12 , Andrew Trevelyan 13 , Holger Volk 14 , Matthew Walker 15 , Neil Yates 16 , Mark J. Prescott 1 1 National Centre for Replacement, Refinement and Reduction of Animals in Research (NC3Rs), Gibbs Building, 215 Euston Road, London, NW1 2BE, UK 2 Department of Pharmacology, University of Oxford, Oxford, OX1 3QT, UK 3 Institute of Neuropathology, University of Erlangen, Erlangen, Germany 4 Neuroscience Division, School of Biosciences, Cardiff University, Cardiff, UK 5 Comparative Biology Centre, Medical School, Newcastle University, Newcastle Upon Tyne, UK 6 School of Life Sciences, University of Warwick, Coventry, UK 7 Neuroscience and Mental Health Research Institute, School of Medicine, Cardiff University, UK 8 UCB Pharma, Brussels, Belgium 9 Department of Neurobiology, Institute for Molecular Sciences, University of Eastern Finland, Finland 10 NC3Rs Board, Gibbs Building, 215 Euston Road, London, NW1 2BE, UK 11 UCL School of Pharmacy, University College London, London, UK 12 Department of Medical Sciences, University of Ferrara, Ferrara, Italy 13 Institute of Neuroscience, Medical School, Newcastle University, Newcastle upon Tyne, UK 14 Department of Clinical Science and Services, The Royal Veterinary College, Hatfield, Herts, UK 15 Institute of Neurology, University College London, London, UK 16 School of Biomedical Sciences, University of Nottingham, Nottingham UK * Corresponding author details – Dr Katie Lidster, National Centre for Replacement, Refinement and Reduction of AnimalsAccepted in Research (NC3Rs), Gibbs Bui Manuscriptlding, 215 Euston Road, London, NW1 2BE, UK. Email: [email protected] . All authors are members of the NC3Rs working group on mammalian models of epilepsy (www.nc3rs.org.uk/epilepsy ). Keywords : 3Rs, animal model, epilepsy, mouse, rat, refinement, seizure. 1 Report of a Working Group of the National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs). Page 1 of 102 Lidster et al. 2 Abstract Animal models of epilepsy and seizures, mostly involving mice and rats, are used to understand the pathophysiology of the different forms of epilepsy and their comorbidities, to identify biomarkers, and to discover new antiepileptic drugs and treatments for comorbidities. Such models represent an important area for application of the 3Rs (replacement, reduction and refinement of animal use). This report provides background information and recommendations aimed at minimising pain, suffering and distress in rodent models of epilepsy and seizures in order to improve animal welfare and optimise the quality of studies in this area. The report includes practical guidance on principles of choosing a model, induction procedures, in vivo recordings, perioperative care, welfare assessment, humane endpoints, social housing, environmental enrichment, reporting of studies and data sharing. In addition, some model-specific welfare considerations are discussed, and data gaps and areas for further research are identified. The guidance is based upon a systematic review of the scientific literature, survey of the international epilepsy research community, consultation with veterinarians and animal care and welfare officers, and the expert opinion and practical experience of the members of a Working Group convened by the United Kingdom’s National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs). Accepted Manuscript Page 2 of 102 Lidster et al. 3 1. Introduction 1.1 Background Epilepsy (see Glossary) is one of the most common serious neurological diseases. It affects an estimated 1% of the population, which equates to about 60 million individuals worldwide (England et al. 2012). Epilepsy patients experience debilitating seizures (see Glossary) associated with abnormal electrical activity in the brain. Seizures typically last tens of seconds to a few minutes, and usually are separated by prolonged interictal periods. Epilepsy does more than cause seizures, however: depending on the type of epilepsy it may be associated with increased mortality (Sillanpää and Shinnar 2010), transient postictal behavioural changes and a range of comorbidities including cognitive impairments (Inostroza et al. 2011), anxiety (Mazarati et al. 2009; Epps and Weinshenker 2013) and systemic effects. At least 15 different types of seizures and 30 epilepsy syndromes have been identified across the lifespan (Berg et al. 2010). The diversity of clinical epilepsies has led to classification by the International League Against Epilepsy (Berg and Cross 2010; Berg and Scheffer 2011). There remain many unresolved clinical issues in epilepsy (Baulac and Pitkänen 2008; Galanopoulou et al. 2012). First, none of the anti-epileptic drugs in clinical use can prevent developmentAccepted of epilepsy in cases Manuscript where the precipitating epileptogenic event is identifiable. Second, pharmacological therapy remains unsatisfactory: one third of the patients treated with antiepileptic drugs continue to experience seizures. In patients in whom seizures are well controlled, drugs may exert debilitating side effects and, in some cases, refractoriness to their therapeutic effects may develop. Page 3 of 102 Lidster et al. 4 Third, disease-modifying therapies are needed: antiepileptic drugs do not prevent the progression of the disease, and there is a lack of therapies that can ameliorate or prevent the associated cognitive, neurological and psychiatric comorbidities, or the epilepsy-related mortality. There is an increased demand for animal models that adequately recapitulate human epilepsy, to further understand the mechanisms underlying epileptogenesis in the different forms of epilepsy (Loscher and Brandt 2010) and to develop therapies to prevent the epileptogenic process, better treat comorbidities and treat drug resistant epilepsy (Baulac and Pitkänen 2008; Brooks-Kayal et al. 2013). However, animal models of epilepsy and seizures, mostly involving mice and rats, have the potential to cause pain, suffering, distress and lasting harm2 to the animals involved. This can be as a consequence of the method of induction of the epilepsy syndrome, comorbidities and associated animal husbandry practices, acute or chronic post-ictal sequelae and instrumentation, and procedures for monitoring epileptiform activity. Hence such models are typically classified in legislation (e.g. the European Directive on the protection of animals used for scientific purposes (2010/63/EU)) as moderate or severe procedures; similar regulations apply elsewhere. There is therefore a need for clear guidance on their use and refinement, in order to minimise any suffering, which is important for ethical, scientific, and legal reasons. 1.2 Working groupAccepted aims and scope Manuscript The National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs) is a scientific organisation established by the United Kingdom (UK) Government in 2004 to lead the discovery and application of new technologies 2 Herein referred to as harms. Page 4 of 102 Lidster et al. 5 and approaches to replace, reduce and refine the use of animals for scientific purposes. In 2013 the NC3Rs convened an expert Working Group with the following terms of reference: 1. To review and summarise current use of mammalian models of epilepsy. 2. To identify the animal welfare issues. 3. To recommend opportunities for refinement. 4. To assess and balance the benefits of epilepsy research against the harms to the animals involved. 5. To publish the deliberations of the Working Group in a peer-reviewed paper and promote the group’s recommendations within the international epilepsy research community. Membership of the Working Group comprised neuroscientists, neurologists, epileptologists, neuropathologists,
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