Is animal research sufficiently evidence based to be a cornerstone of biomedical research?

BMJ (Online)

Volumn 348, Issue , 2014, Pages

  Pound, Pandora ^a   Bracken, Michael B ^b  

^a Yale University Schools of Public Health and Medicine ^*

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CEREBROVASCULAR ACCIDENT; CLINICAL PRACTICE; CLINICAL RESEARCH; EVIDENCE BASED MEDICINE; EXPERIMENTAL ANIMAL; EXPERIMENTAL DESIGN; HUMAN; INVESTMENT; MEDICAL PRACTICE; MEDICAL RESEARCH; NONHUMAN; PRIORITY JOURNAL; PUBLICATION; QUALITATIVE RESEARCH; STATISTICAL ANALYSIS; TRANSGENIC ANIMAL; ANIMAL; ANIMAL EXPERIMENT; PROCEDURES; STANDARDS; UNITED KINGDOM;

ANIMAL EXPERIMENTATION; ANIMALS; BIOMEDICAL RESEARCH; EVIDENCE-BASED MEDICINE; GREAT BRITAIN;

EID: 84901706695     PISSN: None     EISSN: 17561833     Source Type: Journal    
DOI: 10.1136/bmj.g3387     Document Type: Article

References (55)

1. Matthews R. Medical progress depends on animal models-doesn't it? J R Soc Med 2008;101:95-8. (Pubitemid 351498389)
2. Pound P, Ebrahim S, Sandercock P, Bracken M, Roberts I. Where is the evidence that animal research benefits humans? BMJ 2004;328:514-7. (Pubitemid 38293622)
3. Chalmers I, Glasziou P. Avoidable waste in the production and reporting of research evidence. Lancet 2009;374:869.
4. Sandercock P, Roberts I. Systematic reviews of animal experiments. Lancet 2002;360:586. (Pubitemid 35232189)
5. Bracken MB. Risk chance and causation: investigating the origins and treatment of disease. Yale University Press, 2013.
6. Korevaar D, Hooft L, ter Riet G. Systematic reviews and meta-analyses of preclinical studies: publication bias in laboratory animal experiments. Lab Anim 2011;45:225-30.
7. Van Luijk J, Leenaars M, Hooijmans C, Wever K, de Vries R, Ritskes-Hoitinga M. Towards evidence-based translational research: the pros and cons of conducting systematic reviews of animal studies. Altex 2012;30:256-7.
8. Kimmelman J, London AJ. Predicting harms and benefits in translational trials: ethics, evidence and uncertainty. PLoS Med 2011;8:e1001010.
9. Henderson B, Kimmelman J, Fergusson D, Grimshaw J, Hackam D. Threats to validity in the design and conduct of preclinical efficacy studies: a systematic review of guidelines for in vivo animal experiments. PLoS Med 2013;10:e1001489.
10. Kilkenny C, Parsons N, Kadyszewski E, Festing MFW, Cuthill IC, Fry D, et al. Survey of the quality of experimental design, statistical analysis and reporting of research using animals. PLoS ONE 2009;4:e7824.
11. Tsilidis K, Panagiotou O, Sena E, Aretouli E, Evangelou E, Howells D, et al. Evaluation of excess significance bias in animal studies of neurological diseases. PLoS Biol 2013;11:e1001609.
12. Perel P, Roberts I, Sena E, Wheble P, Briscoe C, Sandercock P, et al. Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ 2007;334:197.
13. Sena ES, Bart van der Worp H, Bath PMW, Howells DW, Macleod MR. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol 2010;8:1-8.
14. Ioannidis JPA. Extrapolating from animals to humans. Sci Translat Med 2012;4:1-3.
15. Lindner MD. Clinical attrition due to biased preclinical assessments of potential efficacy. Pharmacol Ther 2007;115:148-75. (Pubitemid 46992811)
16. Hackam DG. Translating animal research into clinical benefit. BMJ 2007;334:163-4. (Pubitemid 46198080)
17. Wall RJ, Shani M. Are animal models as good as we think? Theriogenology 2008;69:2-9. (Pubitemid 350166509)
18. Kimmelman J, Anderson JA. Should preclinical studies be registered? Nature Biotech 2012;30:488-9.
19. Muhlhausler BS, Bloomfield FH, Gillman MW. Whole animal experiments should be more like human randomized controlled trials. PLoS Biol 2013;11:e1001481.
20. Hackam DG, Redelmeier DA. Translation of research evidence from animals to humans. JAMA 2006;296:1731-2. (Pubitemid 44547792)
21. Geerts H. Of mice and men. Bridging the translational disconnect in CNS drug discovery. CNS Drugs 2009;23:915-26.
22. Kola I, Landis J. Can the pharmaceutical industry reduce attrition rates? Nature Rev Drug Discovery 2004;3:711-5. (Pubitemid 39173511)
23. Contopoulos-Ioannidis DG, Ntzani EE, Ioannidis JPA. Translation of highly promising basic science research into clinical applications. Am J Med 2003;114:477-84. (Pubitemid 36515110)
24. Bart van der Worp H, Howells DW, Sena ES, Porritt MJ, Rewell S, O'Collins V, et al. Can animal models of disease reliably inform human studies? PLoS Med 2010;7:e1000245.
25. Sutherland BA, Minnerup J, Balami JS, Arba F, Buchan AM, Kleinschnitz C. Neuroprotection for ischaemic stroke: translation from the bench to the bedside. Int J Stroke 2012;7:407-18.
26. Perrin P. Make mouse studies work. Nature 2014;507:423-5.
27. Seok J, Warren S, Cuenca A, Mindrinos M, Baker H, Xu W, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci 2013;110:3507-12.
28. Chalmers I, Bracken MB, Djulbegovic B, Garattini S, Grant J, Metin Gulmezoglu A, et al. How to increase value and reduce waste when research priorities are set. Lancet 2014;338:156-65.
29. Wooding S, Pollitt A, Castle-Clarke S, Cochrane G, Diepeveen S, Guthrie S, et al. Mental health retrosight: identifying the attributes of successfully translated research (lessons from schizophrenia). 2013. www.rand.org/pubs/ research-briefs/RB9738.
30. Wooding S, Hanney S, Pollitt A, Buxton M, Grant J. Project retrosight: understanding the returns from cardiovascular and stroke research. 2011. www.rand.org/pubs/research-briefs/RB9573.
31. Home Office. Annual statistics of scientific procedures on living animals. Stationery Office, 2012.
32. US Food and Drug Administration. Innovation or stagnation. Challenge and opportunity on the critical path to new medical products. US Department of Health and Human Services, 2004.
33. Hartung T. Look back in anger-what clinical studies tell us about preclinical work. Altex 2014;30:275-91.
34. Understanding Animal Research. Expert and independent opinion. www.understandinganimalresearch.org.uk/resources/expert-and-independent-opinion.
35. Centre for Evidence Based Medicine. Levels of evidence. 2009. www.cebm.net/?o=1025.
36. Shanks N, Greek R. Animal models in light of evolution. BrownWalker, 2009.
37. Leist M, Hartung T. Inflammatory findings on species extrapolations: humans are definitely no 70-kg mice. Arch Toxicol 2013;87:563-67.
38. Boffelli D, Martin DI. Epigenetic inheritance: a contributor to species differentiation? DNA Cell Biol 2012;31:S11-6.
39. Shanks N, Greek R. Experimental use of nonhuman primates is not a simple problem. Nature Med 2008;14:1012-13.
40. Bailey J. Lessons from chimpanzee-based research on human disease: the implications of genetic differences. Altern Lab Anim 2011;39:527-40.
41. Eastwood D, Findlay L, Poole S, Bird C, Wadhwa M, Moore M, et al. Monoclonal antibody TGN1412 trial failure explained by species differences in CD28 expression on CD4+ effector memory T-cells. Br J Pharmacol 2010;161:512-26.
42. Greek R, Menache A. Systematic reviews of animal models: methodology versus epistemology. Int J Med Sci 2013;10:206-21.
43. Lin JH. Applications and limitations of genetically modified mouse models in drug discovery and development. Current Drug Metab 2008;9:419-38. (Pubitemid 352025196)
44. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman D. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010;8:e1000412.
45. Baker D, Lidster K, Sottomayor A, Amor S. Two years later: journals are not yet enforcing the ARRIVE guidelines on reporting standards for pre-clinical animal studies. PLoS Biol 2014;12:e001756.
46. Hooijmans CR, Leenaars M, Ritskes-Hoitinga M. A gold standard publication checklist to improve the quality of animal studies, to fully integrate the three Rs, and to make systematic reviews more feasible. Altern Lab Animal 2010;38:167-82.
47. Festing MFW. We are not born knowing how to design and analyse scientific experiments. Altern Lab Animal 2013;41:1-3.
48. Collins FS, Tabak LA. NIH plans to enhance reproducibility. Nature 2014;505:612-3.
49. Morgan M, Barry C, Donovan J, Sandall J, Wolfe CDA, Boaz Al. Implementing translational biomedical research: convergence and divergence among clinical and basic scientists. Soc Sci Med 2011;73:945-52.
50. Chen Z, Cheng K, Walton Z, Wang Y, Ebi H, Shimamura T, et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 2012;483:613-7.
51. Wendler A, Wehling M. Translatability scoring in drug development: eight case studies. J Transl Med 2012;10:39.
52. Hawkes N. Initiative aims to make London Europe's commercial centre for life sciences. BMJ 2014;348:g2687.
53. Macleod MR, Michie S, Roberts, I, Dirnagl U, Chalmers I, Ioannidis JPA, et al. Biomedical research: increasing value, reducing waste. Lancet 2014;383:2-6.
54. Dal-Ré R, Ioannidis JP, Bracken MB, Buffler PA, Chan AW, Franco EL, et al. Making prospective registration of observational research a reality. Sci Transl Med 2014;6:224.
55. Brown S. Independent investigation into animal research at Imperial College. 2013. http://brownreport.info/wp-content/uploads/2014/02/The-Brown- Report.pdf.