Pre-clinical

Records, that illustrate progress in the evaluation of animal and other pre-clinical research.


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Park WH (1912)
The role of animal experimentation in the discoveries leading to our present knowledge of the etiology, prevention and cure of diphtheria. JAMA 53:453-459.

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Horn J, Limburg M (2001)
Calcium antagonists for ischemic stroke: a systematic review. Stroke 32:570-6. doi: 10.1161/01.str.32.2.570. PMID: 11157199.

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Sandercock P, Roberts I (2002)
Systematic reviews of animal experiments. Lancet 360:586. DOI:https://doi.org/10.1016/S0140-6736(02)09812-4.

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Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I on behalf of the Reviewing Animal Trials Systematically (RATS) Group (2004)
Where is the evidence that animal research benefits humans? BMJ 328:514–7.

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Perel P, Roberts I, Sena E, Wheble P, Briscoe C, Sandercock S, Macleod M,  Mignini LE, Jayaram P, Khan KS (2007)
Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ 334:197-200.

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Matthews RAJ (2008)
Medical progress depends on animal models – doesn’t it? Journal of the Royal Society of Medicine 101: 95–98. DOI 10.1258/jrsm.2007.070164

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Crossley NA, Sena E, Goehler J, Horn J, van der Worp B, Bath PMW, Macleod M, Dirnagl U (2008)
Empirical Evidence of Bias in the Design of Experimental Stroke Studies; A Metaepidemiologic Approach. Stroke 39:929-34. doi: 10.1161/STROKEAHA.107.498725.

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Hooijmans CR, Tillema A, Leenaars M, Ritskes-Hoitinga M (2010)
Enhancing search efficiency by means of a search filter for finding all studies on animal experimentation in PubMed. Laboratory Animals 44:170-175

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Hooijmans CR, Leenaars M, Ritskes-Hoitinga M (2010)
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 Anim 38:167-82. doi: 10.1177/026119291003800208.

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Sena ES, van der Worp HB, Bath PMW, Howells DW, Macleod MR (2010)
Publication bias in reports of animal Stroke studies leads to major overstatement of efficacy. PLoS Biol 8(3): e1000344. doi:10.1371/journal.pbio.1000344

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Sena ES, Briscoe CL, Howells DW, Donnan GA, Sandercock PA, Macleod MR (2010)
Factors affecting the apparent efficacy and safety of tissue plasminogen activator in thrombotic occlusion models of stroke: systematic review and meta-analysis. Journal of Cerebral Blood Flow and Metabolism 30:1905-13.

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De Vries RB, Hooijmans CR, Tillema A, Leenaars M, Ritskes-Hoitinga M (2011)
A search filter for increasing the retrieval of animal studies in Embase. Laboratory Animals 45:268-70.

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Leenaars M, Ritske-Hoitinga M, Griffin G, Ormandy E. (2011)
Background to the Montréal Declaration on the Synthesis of Evidence to Advance the 3Rs Principles in Science, as Adopted by the 8th World Congress on Alternatives and Animal Use in the Life Sciences, Montréal, Canada, on August 25, 2011. Altex Proceedings, 1/12, Proceedings of WC8.

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Prinz F, Schlange T, Asadullah K (2011)
Believe it or not: how much can we rely on published data on potential drug targets? Nat Rev Drug Discov 10:712.

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Korevaar DA, Hooft L, ter Riet G (2011)
Systematic reviews and meta-analyses of preclinical studies: publication bias in laboratory animal experiments. Laboratory Animals 45: 225–230. DOI: 10.1258/la.2011.010121.

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Begley CG, Ellis LM (2012)
Raise standards for preclinical cancer research. Nature 483:531.

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Martic-Kehl MI,Schibli R, Schubiger PA (2012)
Can animal data predict human outcome? Problems and pitfalls of translational animal research. European Journal of Nuclear Medicine and Molecular Imaging 39:1492–1496. 10.1007/s00259-012-2175-z

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Leenaars M, Hooijmans CR, van Veggel N, ter Riet G, Leeflang M, Hooft L, van der Wilt GJ, Tillema A, Ritskes-Hoitinga M (2012)
A step-by-step guide to systematically identify all relevant animal studies. Laboratory Animals 46:24-31.

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Ioannidis JP (2012)
Extrapolating from animals to humans. Sci Transl Med 4(151):151ps15. doi: 10.1126/scitranslmed.3004631. PMID: 22972841.

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Hooijmans CR, Ritskes-Hoitinga M (2013)
Progress in Using Systematic Reviews of Animal Studies to Improve Translational Research. PLoS Med 10(7): e1001482. doi:10.1371/journal.pmed.1001482.

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De Vries RB, Hooijmans CR, Tillema A, Leenaars M, Ritskes-Hoitinga M (2013)
Letter to the editor. Updated version of the Embase search filter for animal studies. Laboratory Animals 48:88.

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Leist M, Hartung T (2013)
Inflammatory findings on species extrapolations: humans are definitely. no 70-kg mice. Archives of Toxicology 87:563–567. doi: 10.1007/s00204-013-1038-0

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Tsilidis KK, Panagiotou OA, Sena ES, Aretouli E, Evangelou E, Howells DW, Salman RA, Macleod MR, Ioannidis JPA (2013)
Evaluation of excess significance bias in animal studies of neurological diseases. PLoS Biol 11: e1001609. doi:10.1371/journal.pbio.1001609.

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Peers IS, South MC, Ceuppens PR, Bright JD, Pilling E (2014)
Can you trust your animal study data? Nature reviews. Drug discovery. 13. 10.1038/nrd4090-c1.

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Ritskes-Hoitinga M, Leenaars M, Avey M, Rovers M, Scholten R (2014)
Systematic reviews of preclinical animal studies can make significant contributions to health care and more transparent translational medicine. Cochrane Database Syst Rev. 3:ED000078.

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Hooijmans CR, IntHout J, Ritskes-Hoitinga M, Rovers MM (2014)
Meta-analyses of animal studies: an introduction of a valuable instrument to further improve healthcare. ILAR J. 55:418-26.

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Pound P, Bracken M (2014)
Is animal research sufficiently evidence based to be a cornerstone of biomedical research? BMJ 348:g3387 doi: 10.1136/bmj.g3387.

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Sena ES, Currie GL, McCann SK, Macleod MR, Howells DW (2014)
Systematic reviews and meta-analysis of preclinical studies: why perform them and how to appraise them critically. J Cereb Blood Flow Metab 34:737-742. doi:10.1038/jcbfm.2014.28

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Hirst JA, Howick J, Aronson JK, Roberts N, Perera R, Koshiaris C, Heneghan C (2014)
The need for randomization in animal trials: an overview of systematic reviews. PLoS One. 2014 Jun 6;9(6):e98856. doi: 10.1371/journal.pone.0098856.

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Mueller KF, Briel M, Strech D, Meerpohl JJ, Lang B, Motschall E, Gloy V, Lamontagne F, Bassler D (2014)
Dissemination bias in systematic reviews of animal research: a systematic review. PLoS One 9:e116016. doi: 10.1371/journal.pone.0116016.

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Green SB (2015)
Can animal data translate to innovations necessary for a new era of patient-centred and individualised healthcare? Bias in preclinical animal research. BMC Medical Ethics 16:53. DOI 10.1186/s12910-015-0043-7.

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de Vries RBM, Hooijmans CR, Langendam MW, van Luijk J, Leenaars M, Ritskes-Hoitinga M, Wever KE (2015)
A protocol format for the preparation, registration and publication of systematic reviews of animal intervention studies. Evidence-based Preclinical Medicine 1, 1, 1–9, e00007, DOI: 10.1002/ebm2.7.

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Begley CG, Ioannidis JPA (2015)
Reproducibility in Science; Improving the Standard for Basic and Preclinical Research. Circulation Research 116:116–126.

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Henderson VC, Demko N, Hakala A, MacKinnon N, Federico CA, Fergusson D, Kimmelman J (2015)
A meta-analysis of threats to valid clinical inference in preclinical research of sunitinib. eLife 4:e08351. DOI: 10.7554/eLife.08351.

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Ritskes-Hoitinga M (2016)
Public accountability lecture: World day for animals in laboratories. https://www.ritskes-hoitinga.eu/bestanden/Public%20speech%20Ritskes%20final.pdf

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Holman C, Piper SK, Grittner U, Diamantaras AA, Kimmelman J, Siegerink B, Dirnagl U (2016)
Where Have All the Rodents Gone? The Effects of Attrition in Experimental Research on Cancer and Stroke. PLoS Biol 14(1): e1002331. doi:10.1371/journal.pbio.1002331.

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Perlman RL (2016)
Mouse models of human disease: An evolutionary perspective. Evol Med Public Health 21:170-6. doi: 10.1093/emph/eow014.

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Hooijmans CR, de Vries RBM, Ritskes-Hoitinga M, Rovers MM, Leeflang MM, IntHout J, Wever KE, Hooft L, de Beer H, Kuijpers T, Macleod MR, Sena ES, ter Riet G, Morgan RL, Thayer KA, Rooney AA, Guyatt GH, Schünemann HJ, Langendam MW, GRADE Working Group (2018)
Facilitating healthcare decisions by assessing the certainty in the evidence from preclinical animal studies. PLoS One 13:e0187271. doi: 10.1371/journal.pone.0187271.

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Cohen D (2018)
Oxford TB vaccine study calls into question selective use of animal data. BMJ 360:j5845 doi: 10.1136/bmj.j5845

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Pound P, Nicol CJ (2018)
Retrospective harm benefit analysis of pre-clinical animal research for six treatment interventions. . PLoS ONE 13(3): e0193758. https://doi.org/10.1371/journal. pone.0193758.

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Pound P, Ritskes‑Hoitinga M (2018)
Is it possible to overcome issues of external validity in preclinical animal research? Why most animal models are bound to fail. J Transl Med 16:304 https://doi.org/10.1186/s12967-018-1678-1.

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Ritskes-Hoitinga M, Wever K (2018)
Improving the conduct, reporting, and appraisal of animal research. BMJ 360:j4935 doi: 10.1136/bmj.j4935.

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Wieschowski S, Chin WWL, Federico C, Sievers S, Kimmelman J, Strech D (2018)
Preclinical efficacy studies in investigator brochures: Do they enable risk-benefit assessment? PLoS Biol 16:e2004879. https://doi.org/10.1371/journal.pbio.2004879.

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Ritskes-Hoitinga M, van Luijk J (2019)
How can systematic reviews teach us more about the implementation of the 3Rs and animal welfare? Animals 9:1163.

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Leenaars CHC, Kouwenaar C, Stafleu FR, Bleich A, Ritskes-Hoitinga M, de Vries RBM, Meijboom FLB (2019)
Animal to human translation: a systematic scoping review of reported concordance rates. J Transl Med 17:223. https://doi.org/10.1186/s12967-019-1976-2.

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Pound P, Ram R (2020)
Are researchers moving away from animal models as a result of poor clinical translation in the field of stroke? An analysis of opinion papers. BMJ Open Science 4:e100041. doi:10.1136/bmjos-2019-100041

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Vollert J, Schenker E, Macleod M, Bespalov A, Wuerbel H, Michel M, Dirnagl U, Potschka H, Waldron AM, Wever K, Steckler T, van de Casteele T, Altevogt B, Sil A, Rice ASC, The EQIPD WP3 study group members (2020)
Systematic review of guidelines for internal validity in the design, conduct and analysis of preclinical biomedical experiments involving laboratory animals. BMJ Open Science 4:e100046. doi:10.1136/bmjos-2019-100046

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McCormack JP, Holmes DT (2020)
Your results may vary: the imprecision of medical measurements. BMJ 368:m149 doi: 10.1136/bmj.m149

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Ritskes-Hoitinga M, Leenaars C, Beumer W, Roo TC, Stafleu F, Meijboom FLB (2020)
Improving Translation by Identifying Evidence for More Human-Relevant Preclinical Strategies. Animals 10, 1170; doi:10.3390/ani10071170

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Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, Browne WJ, Clark A, Cuthill IC, Dirnagl U, Emerson M, Garner P, Holgate ST, Howells DW, Karp NA, Lazic SE, Lidster K, MacCallum CJ, Macleod M, Pearl EJ, Petersen OH, Rawle F, Reynolds P, Rooney K, Sena ES, Silberberg SD, Steckler T, Würbel H (2020)
The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol 18(7): e3000410. https://doi.org/10.1371/journal.

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Pound P, Ritskes-Hoitinga M (2020)
Can prospective systematic reviews of animal studies improve clinical translation? J Transl Med 18:15. https://doi.org/10.1186/s12967-019-02205-x

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Langendam MW, Magnuson K, Williams AR, Walker VR, Howdeshell KL, Rooney AA Hooijmans CR (2021)
Developing a database of systematic reviews of animal studies. Regulatory Toxicology and Pharmacology Vol 123 (2021) 104940.

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Menon JML, Ritskes-Hoitinga M, Pound P, van Oort E (2021)
The impact of conducting preclinical systematic reviews on researchers and their research: A mixed method case study. PLoS ONE 16(12): e0260619. ttps://doi.org/10.1371/ journal.pone.0260619.

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Dirven H, Vist GE, Bandhakavi S, Mehta J, Fitch SE, Pound P, Ram R, Kincaid B, Leenaars CHC, Chen M, Wright RA, Tsaioun K (2021)
Performance of preclinical models in predicting drug-induced liver injury in humans: a systematic review. Sci Rep 11:6403. doi: 10.1038/s41598-021-85708-2.

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