Proceedings of a workshop to address animal methods bias in scientific publishing
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Abstract
Animal methods bias in scientific publishing is a newly defined type of publishing bias describing a preference for animal-based methods where they may not be necessary or where nonanimal-based methods may already be suitable, which impacts the likelihood or timeliness of a manuscript being accepted for publication. This article covers the output from a workshop between stakeholders in publishing, academia, industry, government, and non-governmental organizations. The intent of the workshop was to exchange perspectives on the prevalence, causes, and impact of animal methods bias in scientific publishing, as well as to explore mitigation strategies. Output from the workshop includes summaries of presentations, breakout group discussions, participant polling results, and a synthesis of recommendations for mitigation. Overall, participants felt that animal methods bias has a meaningful impact on scientific publishing, though more evidence is needed to demonstrate its prevalence. Significant consequences of this bias that were identified include the unnecessary use of animals in scientific procedures, the continued reliance on animals in research – even where suitable nonanimal methods exist, poor rates of clinical translation, delays in publication, and negative impacts on career trajectories in science. Workshop participants offered recommendations for journals, publishers, funders, governments, and other policy makers, as well as the scientific community at large, to reduce the prevalence and impacts of animal methods bias. The workshop resulted in the creation of working groups committed to addressing animal methods bias, and activities are ongoing.
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Akhtar, A. (2015). The flaws and human harms of animal experimentation. Camb Q Healthc Ethics 24, 407-419. doi:10.1017/S0963180115000079
Bai, H., Si, L., Jiang, A. et al. (2022). Mechanical control of innate immune responses against viral infection revealed in a human lung alveolus chip. Nat Commun 13, 1928. doi:10.1038/s41467-022-29562-4
Bailey, J. and Balls, M. (2020). Clinical impact of high-profile animal-based research reported in the UK national press. BMJ Open Sci 4, e100039. doi:10.1136/bmjos-2019-100039
Bailey, J. (2021). Biomedical research must change – But a shift toward human-specific research methods is only part of what is needed. Altern Lab Anim 49, 69-72. doi:10.1177/02611929211030417
Balls, M. (2021). It’s time to include harm to humans in harm-benefit analysis – But how to do it, that is the question. Altern Lab Anim 49, 182-196. doi:10.1177/02611929211062223
Carnesecchi, E., Langezaal, I., Patience, B. et al. (2023). OECD harmonised template 201: Structuring and reporting mechanistic information to foster the integration of new approach methodologies for hazard and risk assessment of chemicals. Regul Toxicol Pharmacol 142, 105426. doi:10.1016/j.yrtph.2023.105426
Chou, D. B., Frismantas, V., Milton, Y. et al. (2020). On-chip recapitulation of clinical bone marrow toxicities and patient-specific pathophysiology. Nat Biomed Eng 4, 394-406. doi:10.1038/s41551-019-0495-z
DeVito, N. J. and Goldacre, B. (2019). Catalogue of bias: Publication bias. BMJ Evid Based Med 24, 53-54. doi:10.1136/bmjebm-2018-111107
EC – European Commission, Joint Research Centre (2021). A survey on monitoring innovation and societal impact of EU-funded biomedical research: Synopsis report. LU: Publications Office of the European Union. https://data.europa.eu/doi/10.2760/644131
Ewart, L., Apostolou, A., Briggs, S. A. et al. (2021). Qualifying a human liver-chip for predictive toxicology: Performance assessment and economic implications. bioRxiv, 2021.12.14.472674. doi:10.1101/2021.12.14.472674
Goyal, G., Prabhala, P., Mahajan, G. et al. (2022). Ectopic lymphoid follicle formation and human seasonal influenza vaccination responses recapitulated in an organ-on-a-chip. Adv Sci 9, e2103241. doi:10.1002/advs.202103241
Hamm, J., Sullivan, K., Clippinger, A. J. et al. (2017). Alternative approaches for identifying acute systemic toxicity: Moving from research to regulatory testing. Toxicol In Vitro 41, 245-259. doi:10.1016/j.tiv.2017.01.004
Hassell, B. A., Goyal, G., Lee, E. et al. (2017). Human organ chip models recapitulate orthotopic lung cancer growth, therapeutic responses, and tumor dormancy in vitro. Cell Rep 21, 508-516. doi:10.1016/j.celrep.2017.09.043
Herland, A., Maoz, B. M., Das, D. et al. (2020). Quantitative prediction of human pharmacokinetic responses to drugs via fluidically coupled vascularized organ chips. Nat Biomed Eng 4, 421-436. doi:10.1038/s41551-019-0498-9
Huh, D., Matthews, B. D., Mammoto, A. et al. (2010). Reconstituting organ-level lung functions on a chip. Science 328, 1662-1668. doi:10.1126/science.1188302
Hyman, S. E. (2012). Revolution stalled. Sci Transl Med 4, 155cm11. doi:10.1126/scitranslmed.3003142
Ingber, D. E. (2020). Is it time for reviewer 3 to request human organ chip experiments instead of animal validation studies? Adv Sci 7, 2002030. doi:10.1002/advs.202002030
Ingber, D. E. (2022). Human organs-on-chips for disease modelling, drug development and personalized medicine. Nat Rev Genet 23, 467-491. doi:10.1038/s41576-022-00466-9
Jang, K.-J., Otieno, M. A., Ronxhi, J. et al. (2019). Reproducing human and cross-species drug toxicities using a liver-chip. Sci Transl Med 11, eaax5516. doi:10.1126/scitranslmed.aax5516
Kasendra, M., Tovaglieri, A., Sontheimer-Phelps, A. et al. (2018). Development of a primary human small intestine-on-a-chip using biopsy-derived organoids. Sci Rep 8, 2871. doi:10.1038/s41598-018-21201-7
Krebs, C. E., Lam, A., McCarthy, J. et al. (2023). A survey to assess animal methods bias in scientific publishing. ALTEX 40, 665-676. doi:10.14573/altex.2210212
Lee, C. J., Sugimoto, C. R., Zhang, G. et al. (2013). Bias in peer review. J Am Soc Inf Sci Technol 64, 2-17. doi:10.1002/asi.22784
Leenaars, C. H. C., Kouwenaar, C., Stafleu, F. R. et al. (2019). Animal to human translation: A systematic scoping review of reported concordance rates. J Transl Med 17, 223. doi:10.1186/s12967-019-1976-2
Meigs, L., Smirnova, L., Rovida, C. et al. (2018). Animal testing and its alternatives – The most important omics is economics. ALTEX 35, 275-305. doi:10.14573/altex.1807041
Menon, J. M. L., Ritskes-Hoitinga, M., Pound, P. et al. (2021). The impact of conducting preclinical systematic reviews on researchers and their research: A mixed method case study. PLoS One 16, e0260619. doi:10.1371/journal.pone.0260619
Novak, R., Ingram, M., Marquez, S. et al. (2020). Robotic fluidic coupling and interrogation of multiple vascularized organ chips. Nat Biomed Eng 4, 407-420. doi:10.1038/s41551-019-0497-x
Paini, A. (2012). Generation of in vitro data to model dose dependent in vivo DNA binding of genotoxic carcinogens and its consequences: The case of estragole. Wageningen, NL: Wageningen University.
Pound, P., Ebrahim, S., Sandercock, P. et al. (2004). Where is the evidence that animal research benefits humans? BMJ 328, 514-517. doi:10.1136/bmj.328.7438.514
Ritskes-Hoitinga, M. and Pound, P. (2022). The role of systematic reviews in identifying the limitations of preclinical animal research, 2000-2022: Part 2. J R Soc Med 115, 231-235. doi:10.1177/01410768221100970
Ritskes-Hoitinga, M., Barella, Y. and Kleinhout-Vliek, T. (2022). The promises of speeding up: Changes in requirements for animal studies and alternatives during COVID-19 vaccine approval – A case study. Animals 12, 1735. doi:10.3390/ani12131735
Si, L., Bai, H., Oh, C. Y. et al. (2021). Clinically relevant influenza virus evolution reconstituted in a human lung airway-on-a-chip. Microbiol Spectr 9, e00257-21. doi:10.1128/Spectrum.00257-21
Sontheimer-Phelps, A., Chou, D. B., Tovaglieri, A. et al. (2020). Human colon-on-a-chip enables continuous in vitro analysis of colon mucus layer accumulation and physiology. Cell Mol Gastroenterol Hepatol 9, 507-526. doi:10.1016/j.jcmgh.2019.11.008
Swaters, D., van Veen, A., van Meurs, W. et al. (2022). A history of regulatory animal testing: What can we learn? Altern Lab Anim 50, 322-329. doi:10.1177/02611929221118001
Tomkins, A., Zhang, M. and Heavlin, W. D. (2017). Reviewer bias in single- versus double-blind peer review. Proc Natl Acad Sci U S A 114, 12708-12713. doi:10.1073/pnas.1707323114