Mapping strategies towards improved external validity in preclinical translational research

References

• Leenaars CHC, Kouwenaar C, Stafleu FR, et al. Animal to human translation: a systematic scoping review of reported concordance rates. J Transl Med. 2019;17:223. doi: 10.1186/s12967-019-1976-2
   PubMed Web of Science ®Google Scholar
• Goodman SN, Fanelli D, Ioannidis JPA. What does research reproducibility mean? Sci Transl Med. 2016;8:341. doi: 10.1126/scitranslmed.aaf5027
   Web of Science ®Google Scholar
• Jarvis MF, Williams M. Irreproducibility in preclinical biomedical research: perceptions, uncertainties, and knowledge gaps. Trends Pharmacol Sci. 2016;37:290–302. doi: 10.1016/j.tips.2015.12.001
   PubMed Web of Science ®Google Scholar
• Bishop D. Rein in the four horsemen of irreproducibility. Nature. 2019;568:435–435. doi: 10.1038/d41586-019-01307-2
   PubMed Web of Science ®Google Scholar
• Dirnagl U, Bannach-Brown A, McCann S. External validity in translational biomedicine: understanding the conditions enabling the cause to have an effect. EMBO Mol Med. 2022;14:e14334. doi: 10.15252/emmm.202114334
   PubMed Web of Science ®Google Scholar
• Vollert J, Schenker E, Macleod M, et al. Systematic review of guidelines for internal validity in the design, conduct and analysis of preclinical biomedical experiments involving laboratory animals. BMJ Open Sci. 2020;4:e100046. doi: 10.1136/bmjos-2019-100046
   PubMedGoogle Scholar
• Drude NI, Gamboa LM, Danziger M, et al. Science forum: improving preclinical studies through replications. Elife. 2021;10:e62101. doi: 10.7554/eLife.62101
   PubMed Web of Science ®Google Scholar
• Lesko CR, Ackerman B, Webster-Clark M, et al. Target validity: bringing treatment of external validity in line with internal validity. Curr Epidemiol Rep. 2020;7:117–124. doi: 10.1007/s40471-020-00239-0
   PubMedGoogle Scholar
• Punt A, Bouwmeester H, Blaauboer BJ, et al. New approach methodologies (NAMs) for human-relevant biokinetics predictions: meeting the paradigm shift in toxicology towards an animal-free chemical risk assessment. ALTEX. 2020;37:607–622. doi: 10.14573/altex.2003242
   PubMedGoogle Scholar
• Stucki AO, Barton-Maclaren TS, Bhuller Y, et al. Use of new approach methodologies (NAMs) to meet regulatory requirements for the assessment of industrial chemicals and pesticides for effects on human health. Front Toxicol. 2022;4:964553. doi: 10.3389/ftox.2022.964553
   PubMedGoogle Scholar
• Crabbe JC, Wahlsten D, Dudek BC. Genetics of mouse behavior: Interactions with laboratory environment. Science. 1999;284(5420):1670. doi: 10.1126/science.284.5420.1670
   PubMed Web of Science ®Google Scholar
• van der Staay FJ, Steckler T, van der Staay FJ. Behavioural phenotyping of mouse mutants. Behav Brain Res. 2001;125:3–12. doi: 10.1016/S0166-4328(01)00278-9
   PubMed Web of Science ®Google Scholar
• Würbel H. Behaviour and the standardization fallacy. Nat Genet. 2000;26(3):263–263. doi: 10.1038/81541
   PubMed Web of Science ®Google Scholar
• Richter SH, Garner JP, Würbel H. Environmental standardization: cure or cause of poor reproducibility in animal experiments? Nat Methods. 2009;6(4):257–261. doi: 10.1038/nmeth.1312
   PubMed Web of Science ®Google Scholar
• Wahlsten D. Standardizing tests of mouse behavior: reasons, recommendations, and reality. Physiol Behav. 2001;73:695–704. doi: 10.1016/S0031-9384(01)00527-3
   PubMed Web of Science ®Google Scholar
• Voelkl B, Altman NS, Forsman A, et al. Reproducibility of animal research in light of biological variation. Nat Rev Neurosci. 2020;21:384–393. doi: 10.1038/s41583-020-0313-3
   PubMed Web of Science ®Google Scholar
• Josef van der Staay F., Arndt SS, Nordquist RE, et al. The standardization–generalization dilemma: a way out. Genes Brain Behav. 2010;9:849–855. doi: 10.1111/j.1601-183X.2010.00628.x
   PubMed Web of Science ®Google Scholar
• Witjes VM, Boleij A, Halffman W. Reducing versus Embracing variation as strategies for reproducibility: the microbiome of laboratory mice. Animals. 2020;10:2415. doi: 10.3390/ani10122415
   Web of Science ®Google Scholar
• van der Staay FJ, van der Staay FJ. Animal models of behavioral dysfunctions: basic concepts and classifications, and an evaluation strategy. Brain Res Rev. 2006;52:131–159. doi: 10.1016/j.brainresrev.2006.01.006
   PubMed Web of Science ®Google Scholar
• Würbel H, Garner JP. Refinement of rodent research through environmental enrichment and systematic randomization. NC3Rs. 2007;9:9.
   Google Scholar
• Der Staay FJV, Steckler T. The fallacy of behavioral phenotyping without standardisation. Genes Brain Behav. 2002;1:9–13. doi: 10.1046/j.1601-1848.2001.00007.x
   PubMed Web of Science ®Google Scholar
• Richter SH. Systematic heterogenization for better reproducibility in animal experimentation. Lab Anim. 2017;46:343–349. doi: 10.1038/laban.1330
   Web of Science ®Google Scholar
• Bodden C, von Kortzfleisch VT, Karwinkel F, et al. Heterogenising study samples across testing time improves reproducibility of behavioural data. Sci Rep. 2019;9:8247. doi: 10.1038/s41598-019-44705-2
   PubMed Web of Science ®Google Scholar
• Buch T, Moos K, Ferreira FM, et al. Benefits of a factorial design focusing on inclusion of female and male animals in one experiment. J Mol Med. 2019;97:871–877. doi: 10.1007/s00109-019-01774-0
   PubMed Web of Science ®Google Scholar
• Gur E, Waner T. The variability of organ weight background data in rats. Lab Anim. 1993;27:65–72. doi: 10.1258/002367793781082368
   PubMed Web of Science ®Google Scholar
• André V, Gau C, Scheideler A, et al. Laboratory mouse housing conditions can be improved using common environmental enrichment without compromising data. PLoS Biol. 2018;16:e2005019. doi: 10.1371/journal.pbio.2005019
   PubMed Web of Science ®Google Scholar
• Lewejohann L, Reinhard C, Schrewe A, et al. Environmental bias? Effects of housing conditions, laboratory environment and experimenter on behavioral tests. Genes Brain Behav. 2006;5:64–72. doi: 10.1111/j.1601-183X.2005.00140.x
   PubMed Web of Science ®Google Scholar
• Paylor R. Questioning standardization in science. Nat Methods. 2009;6:253–254. doi: 10.1038/nmeth0409-253
   PubMed Web of Science ®Google Scholar
• Lewejohann L, Zipser B, Sachser N. Personality” in laboratory mice used for biomedical research: A way of understanding variability? Dev Psychobiol. 2011;53:624–630. doi: 10.1002/dev.20553
   PubMed Web of Science ®Google Scholar
• Willmann R, De Luca A, Benatar M, et al. Enhancing translation: Guidelines for standard pre-clinical experiments in mdx mice. Neuromuscular Disorders. 2012;22:43–49. doi: 10.1016/j.nmd.2011.04.012
   PubMed Web of Science ®Google Scholar
• Robinson L, Spruijt B, Riedel G. Between and within laboratory reliability of mouse behaviour recorded in home-cage and open-field. J Neurosci Methods. 2018;300:10–19. doi: 10.1016/j.jneumeth.2017.11.019
   PubMed Web of Science ®Google Scholar
• Corrigan JK, Ramachandran D, He Y, et al. A big-data approach to understanding metabolic rate and response to obesity in laboratory mice. Elife. 2020;9:e53560. doi: 10.7554/eLife.53560
   PubMed Web of Science ®Google Scholar
• Chesler EJ, Wilson SG, Lariviere WR, et al. Influences of laboratory environment on behavior. Nat Neurosci. 2002;5:1101–1102. doi: 10.1038/nn1102-1101
   PubMed Web of Science ®Google Scholar
• Chesler EJ, Wilson SG, Lariviere WR, et al. Identification and ranking of genetic and laboratory environment factors influencing a behavioral trait, thermal nociception, via computational analysis of a large data archive. Neurosci Biobehav Rev. 2002;26:907–923. doi: 10.1016/S0149-7634(02)00103-3
   PubMed Web of Science ®Google Scholar
• Festing MFW. Refinement and reduction through the control of variation. Altern Lab Anim. 2004;32:259–263. doi: 10.1177/026119290403201s43
   PubMed Web of Science ®Google Scholar
• Izídio GS, Lopes DM, Spricigo JL, et al. Common variations in the pretest environment influence genotypic comparisons in models of anxiety. Genes Brain Behav. 2005;4:412–419. doi: 10.1111/j.1601-183X.2005.00121.x
   PubMed Web of Science ®Google Scholar
• Valdar W, Solberg LC, Gauguier D, et al. Genetic and environmental effects on complex Traits in mice. Genetics. 2006;174:959–984. doi: 10.1534/genetics.106.060004
   PubMedGoogle Scholar
• Bailoo JD, Reichlin TS, Würbel H. Refinement of experimental design and conduct in laboratory animal research. ILAR J. 2014;55:383–391. doi: 10.1093/ilar/ilu037
   PubMed Web of Science ®Google Scholar
• Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature. 2014;509:282–283. doi: 10.1038/509282a
   PubMed Web of Science ®Google Scholar
• Miller LR, Marks C, Becker JB, et al. Considering sex as a biological variable in preclinical research. FASEB J. 2017;31:29–34. doi: 10.1096/fj.201600781r
   PubMed Web of Science ®Google Scholar
• Richter SH, Spinello C, Macrì S. Improving External Validity of Experimental Animal Data. In: Martic-Kehl M Schubiger P, editors. Anim Models of Human Cancer. John Wiley & Sons, Ltd; 2016. p. 41–60. doi: 10.1002/9783527695881.ch4
   Google Scholar
• Clayton JA. Applying the new SABV (sex as a biological variable) policy to research and clinical care. Physiol Behav. 2018;187:2–5. doi: 10.1016/j.physbeh.2017.08.012
   PubMed Web of Science ®Google Scholar
• Tannenbaum C, Ellis RP, Eyssel F, et al. Sex and gender analysis improves science and engineering. Nature. 2019;575:137–146. doi: 10.1038/s41586-019-1657-6
   PubMed Web of Science ®Google Scholar
• Usui T, Macleod MR, McCann SK, et al. Meta-analysis of variation suggests that embracing variability improves both replicability and generalizability in preclinical research. PLoS Biol. 2021;19(5):e3001009. doi: 10.1371/journal.pbio.3001009
   PubMed Web of Science ®Google Scholar
• Gärtner K. A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals? Lab Anim. 1990;24:71–77. doi: 10.1258/002367790780890347
   PubMedGoogle Scholar
• Beynen AC, Festing MFW, van Montfort MAJ. Design of animal experiments. In: van Zutphen LFM, Baumans V Beynen AC, editors Principles of laboratory animal science. Elsevier; 2001.
   Google Scholar
• Arroyo-Araujo M, Graf R, Maco M, et al. Reproducibility via coordinated standardization: a multi-center study in a Shank2 genetic rat model for Autism Spectrum Disorders. Sci Rep. 2019;9:11602. doi: 10.1038/s41598-019-47981-0
   PubMed Web of Science ®Google Scholar
• Richter SH, Garner JP, Auer C, et al. Systematic variation improves reproducibility of animal experiments. Nat Methods. 2010;7:167–168. doi: 10.1038/nmeth0310-167
   PubMed Web of Science ®Google Scholar
• Richter SH, Garner JP, Zipser B, et al. Effect of population heterogenization on the reproducibility of mouse behavior: a multi-laboratory study. PLoS One. 2011;6:e16461. doi: 10.1371/journal.pone.0016461
   PubMed Web of Science ®Google Scholar
• Jonker RM, Guenther A, Engqvist L, et al. Does systematic variation improve the reproducibility of animal experiments? Nat Methods. 2013;10:373–373. doi: 10.1038/nmeth.2439
   PubMed Web of Science ®Google Scholar
• Wolfinger RD. Reanalysis of Richter et al.(2010) on reproducibility. Nat Methods. 2013;10:373–374. doi: 10.1038/nmeth.2438
   PubMed Web of Science ®Google Scholar
• Beynen AC, Gärtner K, van Zutphen LFM. Standardization of animal experimentation. In: van Zutphen LFM, Baumans V Beynen AC, editors Principles of laboratory animal science. Elsevier; 2001.
   Google Scholar
• Kafkafi N, Benjamini Y, Sakov A, et al. Genotype–environment interactions in mouse behavior: a way out of the problem. Proc Natl Acad Sci. 2005;102:4619–4624. doi: 10.1073/pnas.0409554102
   PubMed Web of Science ®Google Scholar
• Sundberg JP, Schofield PN. Living inside the box: environmental effects on mouse models of human disease. Dis Model Mech. 2018;11:dmm035360. doi: 10.1242/dmm.035360
   PubMed Web of Science ®Google Scholar
• Servick K. Of mice and microbes. Science. 2016;353:741–743. doi: 10.1126/science.353.6301.741
   PubMed Web of Science ®Google Scholar
• Nigri M, Åhlgren J, Wolfer DP, et al. Role of environment and experimenter in reproducibility of behavioral studies with laboratory mice. Front Behav Neurosci. 2022;16. doi: 10.3389/fnbeh.2022.835444
   PubMed Web of Science ®Google Scholar
• Jaric I, Voelkl B, Clerc M, et al. The rearing environment persistently modulates mouse phenotypes from the molecular to the behavioural level. PLoS Biol. 2022;20:e3001837. doi: 10.1371/journal.pbio.3001837
   PubMed Web of Science ®Google Scholar
• Würbel H. Behavioral phenotyping enhanced – beyond (environmental) standardization. Genes Brain Behav. 2002;1:3–8. doi: 10.1046/j.1601-1848.2001.00006.x
   PubMed Web of Science ®Google Scholar
• Martin LB, Hanson HE, Hauber ME, et al. Genes, environments, and phenotypic Plasticity in Immunology. Trends Immunol. 2021;42:198–208. doi: 10.1016/j.it.2021.01.002
   PubMed Web of Science ®Google Scholar
• von Kortzfleisch VT, Ambrée O, Karp NA, et al. Do multiple experimenters improve the reproducibility of animal studies? PLoS Biol. 2022;20:e3001564. doi: 10.1371/journal.pbio.3001564
   PubMed Web of Science ®Google Scholar
• Georgiou P, Zanos P, Mou T-C, et al. Experimenters’ sex modulates mouse behaviors and neural responses to ketamine via corticotropin releasing factor. Nat Neurosci. 2022;25:1191–1200. doi: 10.1038/s41593-022-01146-x
   PubMed Web of Science ®Google Scholar
• von Kortzfleisch VT, Karp NA, Palme R, et al. Improving reproducibility in animal research by splitting the study population into several ‘mini-experiments’. Sci Rep. 2020;10:16579.
   PubMed Web of Science ®Google Scholar
• Miller VM, Reckelhoff JF. Sex as a biological variable: Now What?! Physiology. 2016;31:78–80. doi: 10.1152/physiol.00058.2015
   PubMed Web of Science ®Google Scholar
• Denfeld QE, Lee CS, Habecker BA. A primer on incorporating sex as a biological variable into the conduct and reporting of basic and clinical research studies. Am J Physiol Heart Circ Physiol. 2022;322:H350–H354. doi: 10.1152/ajpheart.00605.2021
   PubMed Web of Science ®Google Scholar
• Sex in experimental design – MRC [Internet]. UK Research And Innovation. 2022 [cited 2022 Sep 14]. Available from: https://www.ukri.org/councils/mrc/guidance-for-applicants/policies-and-guidance-for-researchers/sex-in-experimental-design/
   Google Scholar
• Collins FS, Tabak LA. Policy: NIH plans to enhance reproducibility. Nature. 2014;505:612–613. doi: 10.1038/505612a
   PubMed Web of Science ®Google Scholar
• Beery AK. Inclusion of females does not increase variability in rodent research studies. Curr Opin Behav Sci. 2018;23:143–149. doi: 10.1016/j.cobeha.2018.06.016
   PubMed Web of Science ®Google Scholar
• Arnegard ME, Whitten LA, Hunter C, et al. Sex as a biological variable: a 5-year progress report and call to action. J Womens Health. 2020;29:858–864. doi: 10.1089/jwh.2019.8247
   PubMed Web of Science ®Google Scholar
• Kretlow JD, Jin Y-Q, Liu W, et al. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol. 2008;9:60. doi: 10.1186/1471-2121-9-60
   PubMed Web of Science ®Google Scholar
• Mazzocca AD, Chowaniec D, McCarthy MB, et al. In vitro changes in human tenocyte cultures obtained from proximal biceps tendon: multiple passages result in changes in routine cell markers. Knee Surg Sports Traumatol Arthrosc. 2012;20:1666–1672. doi: 10.1007/s00167-011-1711-x
   PubMed Web of Science ®Google Scholar
• Dokukin ME, Guz NV, Sokolov I. Mechanical properties of cancer cells depend on number of passages: Atomic force microscopy indentation study. Jpn J Appl Phys. 2017;56:08LB01. doi: 10.7567/JJAP.56.08LB01
   Web of Science ®Google Scholar
• Norden DM, Devine R, McCarthy DO, et al. Storage conditions and passages alter IL-6 secretion in C26 adenocarcinoma cell lines. MethodsX. 2015;2:53–58. doi: 10.1016/j.mex.2015.02.001
   PubMedGoogle Scholar
• Howells DW, Sena ES, Macleod MR. Bringing rigour to translational medicine. Nat Rev Neurol. 2014;10:37–43. doi: 10.1038/nrneurol.2013.232
   PubMed Web of Science ®Google Scholar
• Gagliese L, Melzack R. Age differences in nociception and pain behaviours in the rat. Neurosci Biobehav Rev. 2000;24:843–854. doi: 10.1016/S0149-7634(00)00041-5
   PubMed Web of Science ®Google Scholar
• Barker-Haliski M. How do we choose the appropriate animal model for antiseizure therapy development? Expert Opin Drug Discov. 2019;14:947–951. doi: 10.1080/17460441.2019.1636782
   PubMed Web of Science ®Google Scholar
• Tam WY, Cheung K-K. Phenotypic characteristics of commonly used inbred mouse strains. J Mol Med. 2020;98:1215–1234. doi: 10.1007/s00109-020-01953-4
   PubMed Web of Science ®Google Scholar
• Mekada K, Yoshiki A. Substrains matter in phenotyping of C57BL/6 mice. Exp Anim. 2021;70:145–160. doi: 10.1538/expanim.20-0158
   PubMed Web of Science ®Google Scholar
• Glass AM, Coombs W, Taffet SM. Spontaneous Cardiac Calcinosis in BALB/cByJ mice. Comp Med. 2013;63:29–37.
   PubMed Web of Science ®Google Scholar
• Marchelli JL Strategies to minimize genetic drift and maximize experimental reproducibility in mouse research [Internet]. Charles River Laboratories International, Inc; 2017 [cited 2023 Feb 1]. Available from: https://p.widencdn.net/26bl5m/RM-CS-strategies-to-minimize-genetic-drift-and-maximize-experimental-reproducibility-in-mouse-research.
   Google Scholar
• Colman K. Impact of the genetics and source of preclinical safety animal models on study design, results, and interpretation. Toxicol Pathol. 2017;45:94–106. doi: 10.1177/0192623316672743
   PubMed Web of Science ®Google Scholar
• Biggers JD, Claringbold PJ. Why use inbred lines? Nature. 1954;174:596–597. doi: 10.1038/174596a0
   PubMed Web of Science ®Google Scholar
• Tuttle AH, Philip VM, Chesler EJ, et al. Comparing phenotypic variation between inbred and outbred mice. Nat Methods. 2018;15:994–996. doi: 10.1038/s41592-018-0224-7
   PubMed Web of Science ®Google Scholar
• Festing MFW. Evidence should trump intuition by preferring inbred strains to outbred Stocks in preclinical research. ILAR J. 2014;55:399–404. doi: 10.1093/ilar/ilu036
   PubMed Web of Science ®Google Scholar
• Ratuski AS, Weary DM. Environmental enrichment for rats and mice Housed in laboratories: a metareview. Animals. 2022;12:414. doi: 10.3390/ani12040414
   Web of Science ®Google Scholar
• Official Journal of the European Union. DIRECTIVE 2010/63/EU of the EUROPEAN PARLIAMENT and of the COUNCIL of 22 September 2010 on the protection of animals used for scientific purposes [Internet]. Sep 22, 2010. Available from: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:276:0033:0079:en:PDF
   Google Scholar
• Kentner AC, Speno AV, Doucette J, et al. The Contribution of environmental enrichment to phenotypic variation in mice and rats. eNeuro. 2021;8(2):ENEURO.0539–20.2021. doi: 10.1523/ENEURO.0539-20.2021
   PubMed Web of Science ®Google Scholar
• Nelson RJ, Bumgarner JR, Liu JA, et al. Time of day as a critical variable in biology. BMC Biol. 2022;20:142. doi: 10.1186/s12915-022-01333-z
   PubMed Web of Science ®Google Scholar
• Dallmann R, Okyar A, Lévi F. Dosing-time makes the Poison: Circadian Regulation and Pharmacotherapy. Trends Mol Med. 2016;22:430–445. doi: 10.1016/j.molmed.2016.03.004
   PubMed Web of Science ®Google Scholar
• Fujioka A, Takashima N, Shigeyoshi Y. Circadian rhythm generation in a glioma cell line. Biochem Biophys Res Commun. 2006;346:169–174. doi: 10.1016/j.bbrc.2006.05.094
   PubMed Web of Science ®Google Scholar
• Webb AB, Angelo N, Huettner JE, et al. Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc Natl Acad Sci. 2009;106:16493–16498. doi: 10.1073/pnas.0902768106
   PubMed Web of Science ®Google Scholar
• Sil A, Bespalov A, Dalla C, et al. PEERS — an open science “platform for the exchange of experimental research standards” in biomedicine. Front Behav Neurosci. 2021;15:755812. doi: 10.3389/fnbeh.2021.755812
   PubMed Web of Science ®Google Scholar
• Hair K, Macleod MR, Sena ES, et al. A randomised controlled trial of an intervention to improve compliance with the ARRIVE guidelines (IICARus). Res Integr Peer Rev. 2019;4:12. doi: 10.1186/s41073-019-0069-3
   PubMedGoogle Scholar
• Leung V, Rousseau-Blass F, Beauchamp G, et al. ARRIVE has not ARRIVEd: support for the ARRIVE (animal research: reporting of in vivo experiments) guidelines does not improve the reporting quality of papers in animal welfare, analgesia or anesthesia. PLoS One. 2018;13(5):e0197882. doi: 10.1371/journal.pone.0197882
   PubMed Web of Science ®Google Scholar
• Voelkl B, Würbel H, Krzywinski M, et al. The standardization fallacy. Nat Methods. 2021;18(1):5–7. doi: 10.1038/s41592-020-01036-9
   PubMed Web of Science ®Google Scholar
• Karp NA, Fry D. What is the optimum design for my animal experiment? BMJ Open Sci. 2021;5(1):e100126. doi: 10.1136/bmjos-2020-100126
   PubMedGoogle Scholar
• R Core Team. R: A Language And Environment For Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2021. Available from: https://www.R-project.org/
   Google Scholar
• Zhang Z, Mai Y. WebPower: Basic and Advanced statistical power analysis [Internet]. 2022 [cited 2022 Sep 15]. Available from: https://CRAN.R-project.org/package=WebPower
   Google Scholar
• Sommet N, Weissman DL, Cheutin N, et al. How many participants do i need to test an interaction? Conducting an appropriate power analysis and achieving sufficient power to detect an interaction. OSF Preprints. 2023. Available from. doi: 10.31219/osf.io/xhe3u
   Google Scholar
• Drude N, Martinez-Gamboa L, Danziger M, et al. Planning preclinical confirmatory multicenter trials to strengthen translation from basic to clinical research – a multi-stakeholder workshop report. Trans Med Commun. 2022;7(24). doi: 10.1186/s41231-022-00130-8
   Google Scholar
• Karp NA, Wilson Z, Stalker E, et al. A multi-batch design to deliver robust estimates of efficacy and reduce animal use – a syngeneic tumour case study. Sci Rep. 2020;10:6178. doi: 10.1038/s41598-020-62509-7
   PubMed Web of Science ®Google Scholar
• Hunniford VT, Grudniewicz A, Fergusson DA, et al. A systematic assessment of preclinical multilaboratory studies and a comparison to single laboratory studies [Internet]. OSF Preprints. 2021. Available from. doi: 10.31219/osf.io/92u7d
   Google Scholar
• Voelkl B, Würbel H. A reaction norm perspective on reproducibility. Theory Biosci. 2021;140:169–176. doi: 10.1007/s12064-021-00340-y
   PubMed Web of Science ®Google Scholar
• Voelkl B, Vogt L, Sena ES, et al. Reproducibility of preclinical animal research improves with heterogeneity of study samples. PLoS Biol. 2018;16(2):e2003693. doi: 10.1371/journal.pbio.2003693
   PubMed Web of Science ®Google Scholar
• Nosek BA, Errington TM. What is replication? PLoS Biol. 2020;18(3):e3000691. doi: 10.1371/journal.pbio.3000691
   PubMed Web of Science ®Google Scholar
• Borenstein M, Hedges LV, Higgins JPT, et al. How a meta-analysis works. Introduction to meta-analysis [Internet]. John Wiley & Sons, Ltd; 2009. p. 1–7. doi: 10.1002/9780470743386
   Google Scholar
• Stappenbeck TS, Virgin HW. Accounting for reciprocal host–microbiome interactions in experimental science. Nature. 2016;534:191–199. doi: 10.1038/nature18285
   PubMed Web of Science ®Google Scholar
• Rosshart SP, Herz J, Vassallo BG, et al. Laboratory mice born to wild mice have natural microbiota and model human immune responses. Science. 2019;365:eaaw4361. doi: 10.1126/science.aaw4361
   PubMed Web of Science ®Google Scholar
• Rodrigues J, Heinrich MA, Teixeira LM, et al. 3D in vitro model (R)evolution: unveiling tumor–stroma interactions. Trends Cancer. 2021;7:249–264. doi: 10.1016/j.trecan.2020.10.009
   PubMed Web of Science ®Google Scholar
• Foo MA, You M, Chan SL, et al. Clinical translation of patient-derived tumour organoids- bottlenecks and strategies. Biomark Res. 2022;10:10. doi: 10.1186/s40364-022-00356-6
   PubMed Web of Science ®Google Scholar
• Tang X-Y, Wu S, Wang D, et al. Human organoids in basic research and clinical applications. Sig Transduct Target Ther. 2022;7:1–17. doi: 10.1038/s41392-022-01024-9
   PubMed Web of Science ®Google Scholar
• Kimmelman J, Mogil JS, Dirnagl U, et al. Distinguishing between exploratory and confirmatory preclinical research will improve translation. PLoS Biol. 2014;12(5):e1001863. doi: 10.1371/journal.pbio.1001863
   PubMed Web of Science ®Google Scholar
• Ritskes-Hoitinga M, Leenaars C, Beumer W, et al. Improving translation by Identifying evidence for more human-relevant preclinical strategies. Animals. 2020;10:1170. doi: 10.3390/ani10071170
   Web of Science ®Google Scholar
• Denayer T, Stöhr T, Van Roy M. Animal models in translational medicine: Validation and prediction. New Horizons In Transl Med. 2014;2:5–11. doi: 10.1016/j.nhtm.2014.08.001
   Google Scholar
• Hua S, de Matos MBC, Metselaar JM, et al. Current Trends and challenges in the clinical translation of nanoparticulate nanomedicines: pathways for translational development and commercialization. Front Pharmacol. 2018;9:790. doi: 10.3389/fphar.2018.00790
   PubMed Web of Science ®Google Scholar
• Wagner J, Dahlem AM, Hudson LD, et al. A dynamic map for learning, communicating, navigating and improving therapeutic development. Nat Rev Drug Discov. 2018;17:150–150. doi: 10.1038/nrd.2017.217
   PubMed Web of Science ®Google Scholar
• Danziger M, Dirnagl U, Toelch U. Increasing discovery rates in preclinical research through optimised statistical decision criteria. bioRxiv. 2022. doi: 10.1101/2022.01.17.476585. 2022.01.17.476585.
   Google Scholar
• Heinl C, Scholman-Végh AMD, Mellor D, et al. Declaration of common standards for the preregistration of animal research—speeding up the scientific progress. PNAS Nexus. 2022;1:c016. doi: 10.1093/pnasnexus/pgac016
   Google Scholar
• Candelario-Jalil E, Paul S. Impact of aging and comorbidities on ischemic stroke outcomes in preclinical animal models: a translational perspective. Exp Neurol. 2021;335:113494. doi: 10.1016/j.expneurol.2020.113494
   PubMed Web of Science ®Google Scholar
• Bareham B, Georgakopoulos N, Matas-Céspedes A, et al. Modeling human tumor-immune environments in vivo for the preclinical assessment of immunotherapies. Cancer Immunol Immunother. 2021;70:2737–2750. doi: 10.1007/s00262-021-02897-5
   PubMed Web of Science ®Google Scholar
• du SN, Hurst V, Ahluwalia A, et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol. 2020;18:e3000410. doi: 10.1371/journal.pbio.3000410
   PubMed Web of Science ®Google Scholar
• Carneiro CFD, Queiroz VGS, Moulin TC, et al. Comparing quality of reporting between preprints and peer-reviewed articles in the biomedical literature. Res Integ Peer Rev. 2020;5:16. doi: 10.1186/s41073-020-00101-3
   PubMedGoogle Scholar