Investigation of the publication rate of recent research projects using non-human primates in France
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Abstract
The use of non-human primates (NHPs) in biomedical research entails significant ethical considerations, demanding careful evaluation of both scientific necessity and research outcomes. This study presents a retrospective literature review comparing non-technical summaries (NTS) of research projects authorized in France between 2016 and mid-2019 with corresponding peer-reviewed scientific publications. The primary objective was to assess the publication rate of NHP-based projects, with secondary outcomes including time to publication, discrepancy in animal use reporting, and the scientific impact of published results. Literature searches were conducted primarily via PubMed, supplemented with additional methods such as author-based searches. Out of 191 projects analyzed, 56% led to at least one publication, the publication rate varying markedly, ranging from 83% in ophthalmology to 30% in immunology. In most cases, publications reported fewer animals than originally authorized: 1,751 actually used out of the 3,649 planned. 2,421 animals had been authorized for the projects for which no publication could be identified. The overall median Relative Citation Ratio (RCR), representing the field- and time-normalized citation rate for published studies, was 1.1, indicating a moderate scientific impact. These findings highlight the need for greater transparency in reporting, including the publication of negative or inconclusive results. The study underscores the importance of systematic retrospective assessments, improved harm/benefit evaluations under the EU Directive, and stronger upstream review mechanisms. Key recommendations include pre-registration of studies, mandated publication of all research outcomes, and the development of open-access platforms to facilitate data sharing, reduce unnecessary duplication, and enhance both ethical and scientific value.
Plain language summary
This study examines how often research involving non-human primates (NHPs) in France results in scientific publications. From 2016 to mid-2019, only 56% of such projects led to at least one publication, with wide differences between research areas. Many results from studies are not published, limiting progress and transparency while wasting resources and animal lives. Even when results were published, they often had limited scientific impact. To address this, we recommend better evaluation of research plans, mandatory sharing of all outcomes—including negative results—and more open data systems to improve ethics, transparency and scientific value.
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Chalmers, I., Glasziou, P. (2009). Avoidable waste in the production and reporting of research evidence. Lancet 374, 86-89. doi:10.1016/S0140-6736(09)60329-9
Deutsch, S., Reuter, S., Rose, A. et al. (2020). Publication rates of research projects of an internal funding program of a university medical center in Germany: A retrospective study (2004-2013). PLoS One 15, e0243092. doi:10.1371/journal.pone.0243092
Deutsch, S., Heider, M., Glage, S. et al. (2021). Web-based survey among animal researchers on publication practices and incentives for increasing publication rates. PLoS One 16, e0250362. doi:10.1371/journal.pone.0250362
Dickersin, K. (2006). Publication bias: recognizing the problem, understanding its origins and scope, and preventing harm. In H.R. Roshtein, A.J. Sutton, M. Borenstein (eds.), Publication Bias in Meta-Analysis: Prevention, Assessment, and Adjustments (9-33). John Wiley & Sons. doi:10.1002/0470870168.ch2
EC – European Commission (2018). Working document: Caring for animals aiming for better science – Directive 2010/63/EU on protection of animals used for scientific purposes – Project evaluation and retrospective assessment. Publications Office of the European Union. https://data.europa.eu/doi/10.2779/59814
EU – European Union (2010). 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: https://eur-lex.europa.eu/eli/dir/2010/63/oj
EU (2020). Commission Implementing Decision (EU) 2020/569 of 16 April 2020 establishing a common format and information content for the submission of the information to be reported by Member States pursuant to Directive 2010/63/EU of the European Parliament and of the Council on the protection of animals used for scientific purposes and repealing Commission Implementing Decision 2012/707/EU. https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32020D0569
Gray, R., Bressington, D., Thompson, D. R., Jones, M. (2023). Why Pre-Registration of Research Must Be Taken More Seriously. Nurs Rep 13, 679-681. doi:10.3390/nursrep13020060
Grimm, H., Eggel, M., Deplazes-Zemp, A., Biller-Andorno, N. (2017). The Road to Hell Is Paved with Good Intentions: Why Harm-Benefit Analysis and Its Emphasis on Practical Benefit Jeopardizes the Credibility of Research. Animals (Basel) 7, 70. doi:10.3390/ani7090070
Grimm, H., Olsson, I. A. S., Sandøe, P. (2019). Harm-benefit analysis - what is the added value? A review of alternative strategies for weighing harms and benefits as part of the assessment of animal research. Lab Anim 53, 17-27. doi:10.1177/0023677218783004
Hutchins, B. I., Yuan, X., Anderson, J. M. et al. (2016). Relative citation ratio (RCR) : A new metric that uses citation rates to measure influence at the article level. PLoS Biol 14, e1002541. doi:10.1371/journal.pbio.1002541
Ineichen, B. V., Furrer, E., Grüninger, S. L. et al. (2024). Analysis of animal-to-human translation shows that only 5% of animal-tested therapeutic interventions obtain regulatory approval for human applications. PLoS Biol 22, e3002667. doi:10.1371/journal.pbio.3002667
Ioannidis, J. P. A., Greenland, S., Hlatky, M. A. et al. (2014). Increasing value and reducing waste in research design, conduct, and analysis. Lancet 383, 166-175. doi: doi:10.1016/S0140-6736(13)62227-8
Koslov, M. (2024). So you got a null result. Will anyone publish it ? Nature 631, 728-730. doi:10.1038/d41586-024-02383-9
Krebs, C. E., Camp, C., Constantino, H. et al. (2023). Author Guide for Addressing Animal Methods Bias in Publishing, Adv Sci 10, e2303226. doi:10.1002/advs.202303226
Laber, K., Newcomer, C. E., Decelle, T. et al. (2016). Recommendations for Addressing Harm–Benefit Analysis and Implementation in Ethical Evaluation– Report from the AALAS–FELASA Working Group on Harm–Benefit Analysis– Part 2. Lab Anim 50 Suppl 1, 21-42. doi:10.1177/0023677216642397
Marshall, L. J., Bailey, J., Cassotta, M. et al. (2021). Poor Translatability of Biomedical Research Using Animals — A Narrative Review. Altern Lab Anim 51, 102-135. doi:10.1177/02611929231157756
Nosek, B. A., Ebersole, C. R., DeHaven, A. C. et al. (2018). The preregistration revolution. PNAS 115, 2600-2606. doi:10.1073/pnas.1708274114
Russell, W. M. S., Burch, R. L. (1959). The Principles of Humane Experimental Technique. London: Methuen&Co
Schmucker, C., Schell, L. K., Portalupi, S. et al. (2014). Extent of non-publication in cohorts of studies approved by research ethics committees or included in trial registries. PLoS One 9, e114023. doi:10.1371/journal.pone.0114023
Sena, E. S., van der Worp, H. B., Bath, et al. (2010). Publication Bias in Reports of Animal Stroke Studies Leads to Major Overstatement of Efficacy. PLoS Biol 8, e1000344. doi:10.1371/journal.pbio.1000344
ter Riet, G., Korevaar, D. A., Leenaars, M. et al. (2012). Publication bias in laboratory animal research: a survey on magnitude, drivers, consequences and potential solutions. PLoS One 7, e43404. doi:10.1371/journal.pone.0043404
Thompson, E. A., Loré, K. (2017). Non-human primates as a model for understanding the mechanism of action of toll-like receptor-based vaccine adjuvants. Curr Opin Immunol 47, 1-7. doi:10.1016/j.coi.2017.06.006
van der Naald, M., Wenker, S., Doevendans, P. A. et al. (2020). Publication rate in preclinical research: a plea for preregistration. BMJ Open Science 4, e100051. doi:10.1136/bmjos-2019-100051
Wieschowski, S., Biernot, S., Deutsch, S. et al. (2019). Publication rates in animal research. Extent and characteristics of published and non-published animal studies followed up at two German university medical centres. PLoS One 14, e0223758. doi:10.1371/journal.pone.0223758
Wong, C. H., Siah, K. W., Lo, A. W. (2019). Estimation of clinical trial success rates and related parameters. Biostatistics 20, 273-286. doi:10.1093/biostatistics/kxx069