Educational use of animals in Europe indicates a reluctance to implement alternatives

Main Article Content

Miriam A. Zemanova
Andrew Knight
Susanna Lybæk

Abstract

Animals have been considered an indispensable tool to teach about the functioning of living organisms, to obtain skills necessary for practicing human and veterinary medicine, as well as for acquiring skills for caring for and conducting experiments on animals in laboratories. However, the efficacy of this practice has been questioned in the last decades and societal views have evolved to put a much larger emphasis on animal welfare and ethics that needs to be reflected in our teaching and training practices. Currently, many alternatives to harmful animal use are available, and it is not clear why thousands of animals continue to be used every year for educational and training purposes. Therefore, this study aimed to identify reasons for the lack of uptake of non-harmful educational and training methods by analysing recently published non-technical summaries in the EU and EEA Member States, and to provide examples of alternatives for specific learning objectives. Results from non-technical summaries from 18 countries spanning the most recent years (2017-2019) revealed that the two main perceived reasons for continued animal use are 1) the necessity of using a living animal for ‘proper’ learning and 2) the lack of an adequate alternative. We argue that these reasons often do not reflect reality. In conclusion, we consider it is necessary to put a stronger emphasis on engagement with ethical questions that underlie the use of animals and careful consideration of how the learning objectives could be achieved through non-harmful alternatives.

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How to Cite
Zemanova, M., Knight, A. and Lybæk, S. (2021) “Educational use of animals in Europe indicates a reluctance to implement alternatives”, ALTEX - Alternatives to animal experimentation. doi: 10.14573/altex.2011111.
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References

Abi-Rafeh, J., Zammit, D., Jaberi, M. M. et al. (2019). Nonbiological microsurgery simulators in plastic surgery training: a systematic review. Plast Reconstr Surg 144, 496e-507e. doi:10.1097/PRS.0000000000005990

Aboud, E., Suarez, C. E., Al-Mefty, O. et al. (2004). New alternative to animal models for surgical training. ATLA 32, 501-507. doi:10.1177/026119290403201s80

Aboud, E. T., Aboud, G. and Aboud, T. (2015). “Live cadavers” for practicing airway management. Mil Med 180, 165-170. doi:10.7205/MILMED-D-14-00396

Adams, C. M., Nigrovic, L. E., Hayes, G. et al. (2018). Teaching incision and drainage: perceived educational value of abscess models. Pediatr Emerg Care 34, 174-178. doi:10.1097/PEC.0000000000001240

Akbarsha, M. A. (2007). Movement to curtail animal dissections in zoology curriculum: review of the Indian experience. ALTEX 24, 163-166. doi:10.14573/altex.2007.3.163

Akbarsha, M. A., Zeeshan, M. and Meenakumari, K. J. (2013). Alternatives to animals in education, research, and risk assessment: an overview with special reference to Indian context. ALTEX Proceedings 2, 5-19. doi:10.4103/0253-7613.132153

Al-Elq, A. H. (2010). Simulation-based medical teaching and learning. J Family Community Med 17, 35. doi:10.4103/1319-1683.68787

Arluke, A. and Hafferty, F. (1996). From apprehension to fascination with ''dog lab'': the use of absolutions by medical students. Journal of Contemporary Ethnography 25, 201-225. doi:10.1177/089124196025002002

Atesok, K., Satava, R. M., Marsh, J. L. et al. (2017). Measuring surgical skills in simulation-based training. J Am Acad Orthop Surg 25, 665-672. doi:10.5435/JAAOS-D-16-00253

Aydin, A., Ahmed, K., Van Hemelrijck, M. et al. (2020). LBA01-05 simulation in urological training and education (SIMULATE): an international randomised controlled clinical and educational trial to determine the effect of simulation-based surgical training. The Journal of Urology 203, e1021-e1021. doi:10.1097/JU.0000000000000946.05

Baillie, S., Crossan, A., Brewster, S. A. et al. (2005a). Validation of a bovine rectal palpation simulator for training veterinary students. Stud Health Technol Inform 111, 33-36. http://eprints.gla.ac.uk/3729/

Baillie, S., Mellor, D. J., Brewster, S. A. et al. (2005b). Integrating a bovine rectal palpation simulator into an undergraduate veterinary curriculum. J Vet Med Educ 32, 79-85. doi:10.3138/jvme.32.1.79

Baillie, S., Crossan, A., Brewster, S. A. et al. (2010). Evaluating an automated haptic simulator designed for veterinary students to learn bovine rectal palpation. Simulation in Healthcare 5, 261-266. doi:10.1097/SIH.0b013e3181e369bf

Balls, M. (2018). Replacing animal use in education and training. ATLA 46, 107-108. doi:10.1177/026119291804600303

Balluch, M. (2006). Animals have a right to life. ALTEX 23, 281-286.

Becker, G. J. (2007). Simulation and the coming transformation of medical education and training. Radiology 245, 7-9. doi:10.1148/radiol.2451070674

Bishop, L. J. and Nolen, A. L. (2001). Animals in research and education: ethical issues. Kennedy Inst Ethics J 11, 91-112. doi:10.1353/ken.2001.0006

Bradley, P. (2006). The history of simulation in medical education and possible future directions. Med Educ 40, 254-262. doi:10.1111/j.1365-2929.2006.02394.x

Cagiltay, N. E., Ozcelik, E., Isikay, I. et al. (2019). The effect of training, used-hand, and experience on endoscopic surgery skills in an educational computer-based simulation environment (ECE) for endoneurosurgery training. Surg Innov 26, 725-737. doi:10.1177/1553350619861563

Can, A., Dao, D. T., Terrillion, C. E. et al. (2012). The tail suspension test. JoVE e3769. doi:10.3791/3769

Capaldo, T. (2004). The psychological effects on students of using animals in ways that they see as ethically, morally or religiously wrong. ATLA 32, 525-531. doi:10.1177/026119290403201s85

Cingi, C. C., Baser, D. F., Karafakioglu, Y. S. et al. (2012). Stress response in dairy cows related to rectal examination. Acta Scientiae Veterinariae 40, 1053. https://www.redalyc.org/pdf/2890/289023557008.pdf

Clevenger, J. and Kass, P. H. (2003). Determinants of adoption and euthanasia of shelter dogs spayed or neutered in the University of California veterinary student surgery program compared to other shelter dogs. J Vet Med Educ 30, 372-378. doi:10.3138/jvme.30.4.372

Coombs, C. M., Shields, R. Y., Hunt, E. A. et al. (2017). Design, implementation, and evaluation of a simulation-based clinical correlation curriculum as an adjunctive pedagogy in an anatomy course. Acad Med 92, 494-500. doi:10.1097/ACM.0000000000001387

Crawford, S. B., Huque, Y. I., Austin, D. E. et al. (2019). Development and review of the chest tube high-feedback educational simulation trainer (CHEST). Journal of the Society for Simulation in Healthcare 14, 276-279. doi:10.1097/sih.0000000000000361

Crofts, J. F., Bartlett, C., Ellis, D. et al. (2006). Training for shoulder dystocia: a trial of simulation using low-fidelity and high-fidelity mannequins. Obstet Gynecol 108, 1477-1485. doi:10.1097/01.AOG.0000246801.45977.c8

da Silva, A. P. G., Rodriguez, J. E. R., de Oliveira, M. C. et al. (2019). The alternative model of silicone for experimental simulation of suture of living tissue in the teaching of surgical technique. Acta Cir Bras 34, e201900410. doi:10.1590/s0102-865020190040000010

Davies, J., Khatib, M. and Bello, F. (2013). Open surgical simulation: a review. J Surg Educ 70, 618-627. doi:10.1016/j.jsurg.2013.04.007

de Souza, M. C. C. M. I. and Matera, J. M. (2015). Bleeding simulation in embalmed cadavers: bridging the gap between simulation and live surgery. ALTEX 32, 59-63. doi:10.14573/altex.1407311

De Villiers, R. and Monk, M. (2005). The first cut is the deepest: reflections on the state of animal dissection in biology education. Journal of Curriculum Studies 37, 583-600. doi:10.1080/00220270500041523

Deonarain, A. R., Harrison, R. V., Gordon, K. A. et al. (2020). Live porcine model for surgical training in tracheostomy and open‐airway surgery. The Laryngoscope 130, 2063-2068. doi:10.1002/lary.28309

Dewhurst, D. (2008). Is it possible to meet the learning objectives of undergraduate pharmacology classes with non-animal models? AATEX 14, 207-212. http://www.asas.or.jp/jsaae_old/aatex/Vol12S.html

Draycott, T., Sibanda, T., Owen, L. et al. (2006). Does training in obstetric emergencies improve neonatal outcome? BJOG 113, 177-182. doi:10.1111/j.1471-0528.2006.00800.x

Duhem, H., Viglino, D., Bellier, A. et al. (2019). Cadaver models for cardiac arrest: a systematic review and perspectives. Resuscitation 143, 68-76. doi:10.1016/j.resuscitation.2019.08.009

Durand, M. d. T., Restini, C. B. A., Wolff, A. C. D. et al. (2019). Students’ perception of animal or virtual laboratory in physiology practical classes in PBL medical hybrid curriculum. Adv Physiol Educ 43, 451-457. doi:10.1152/advan.00005.2019

Engel, R. M., Silver, C. C., Veeder, C. L. et al. (2020). Cognitive dissonance in laboratory animal medicine and implications for animal welfare. Journal of the American Association for Laboratory Animal Science 59, 132-138. doi:10.30802/AALAS-JAALAS-19-000073

European Commission (2009). Final report of the expert working group on severity classification of scientific procedures performed on animals. European Commission. https://ec.europa.eu/environment/archives/lab_animals/ewg_en.htm

European Commission (2013). Working document on Non-Technical Project summaries. https://ec.europa.eu/environment/chemicals/lab_animals/pdf/Recommendations%20for%20NTS.pdf

European Commission (2020). 2019 Report on the statistics on the use of animals for scientific purposes in the Member States of the European Union in 2015-2017. Report from the Commission to the European Parliament and the Council. EC.

Feins, R. H., Burkhart, H. M., Conte, J. V. et al. (2017). Simulation-based training in cardiac surgery. The Annals of Thoracic Surgery 103, 312-321. doi:10.1016/j.athoracsur.2016.06.062

Fowler, H. S. and Brosius, E. J. (1968). A research study on the values gained from dissection of animals in secondary school biology. Science Education 52, 55-57. doi:10.1002/sce.3730520114

Gala, S. G. and Crandall, M. L. (2019). Global collaboration to modernize advanced trauma life support training. J Surg Educ 76, 487-496. doi:10.1016/j.jsurg.2018.08.011

Garcia, D. F. V., Domingues, C. A., Collet e Silva, F. S. et al. (2019). Efficacy of a novel surgical manikin for simulating emergency surgical procedures. The American Surgeon 85, 1318-1326. http://observatorio.fm.usp.br/handle/OPI/34256

Gelberg, S. and Gelberg, H. (2005). Stress management interventions for veterinary students. J Vet Med Educ 32, 173-181. doi:10.3138/jvme.32.2.173

Giese, H., Hilke, J., Gundelach, Y. et al. (2015). Validation of a bovine vascular access model for teaching students a technique for placing catheter in the auricular vein of cattle. InVeST Conference 2015, https://www.researchgate.net/publication/283120488_Validation_of_a_bovine_vascular_access_model_for_teaching_students_a_technique_for_placing_catheter_in_the_auricular_vein_of_cattle

Giese, H., Dilly, M., Gundelach, Y. et al. (2018). Influence of transrectal palpation training on cortisol levels and heart rate variability in cows. Theriogenology 119, 238-244. doi:10.1016/j.theriogenology.2018.07.016

Giménez, M. E., Garcia Vazquez, A., Davrieux, C. F. et al. (2020). Image-guided surgical training in percutaneous hepatobiliary procedures: development of a realistic and meaningful bile duct dilatation porcine model. Journal of Laparoendoscopic and Advanced Surgical Techniques doi:10.1089/lap.2020.0680

Graham, J., Alloway, T. and Krames, L. (1994). Sniffy, the virtual rat: simulated operant conditioning. Behav Res Methods Instrum Comput 26, 134-141. doi:10.3758/BF03204606

Grant, J. S., Moss, J., Epps, C. et al. (2010). Using video-facilitated feedback to improve student performance following high-fidelity simulation. Clinical Simulation in Nursing 6, e177-e184. doi:10.1016/j.ecns.2009.09.001

Grevemeyer, B. and Knight, A. (2018). The development of a clinical skills laboratory at Ross University School of Veterinary Medicine. ATLA 46, 177-183. doi:10.1177/026119291804600305

Griswold, S., Ponnuru, S., Nishisaki, A. et al. (2012). The emerging role of simulation education to achieve patient safety: translating deliberate practice and debriefing to save lives. Pediatric Clinics 59, 1329-1340. doi:10.1016/j.pcl.2012.09.004

Guedes, H. G., Câmara Costa Ferreira, Z. M., Ribeiro de Sousa Leão, L. et al. (2019). Virtual reality simulator versus box-trainer to teach minimally invasive procedures: a meta-analysis. International Journal of Surgery 61, 60-68. doi:10.1016/j.ijsu.2018.12.001

Hall, A. B., Riojas, R. and Sharon, D. (2014). Comparison of self-efficacy and its improvement after artificial simulator or live animal model emergency procedure training. Mil Med 179, 320-323. doi:10.7205/milmed-d-12-00446

Hansen, L. A. (2014). Animal laboratories are not needed to train medical students. J Surg Educ 71, 454. doi:10.1016/j.jsurg.2014.02.001

Hardman, J. G. and Ross, J. J. (2006). Modelling: a core technique in anaesthesia and critical care research. Br J Anaesth 97, 589-592. doi:10.1093/bja/ael272

Hart, L. A., Wood, M. W. and Hart, B. L. (2008). Why Dissection? Animal Use in Education. Westport, CT: Greenwood Press.

Hellyer, P., Frederick, C., Lacy, M. et al. (1999). Attitudes of veterinary medical students, house officers, clinical faculty, and staff toward pain management in animals. J Am Vet Med Assoc 214, 238-244. https://europepmc.org/article/med/9926017

Howe, L. M. and Slater, M. R. (1997). Student assessment of the educational benefits of a prepubertal gonadectomy program (preliminary findings). J Vet Med Educ 24, 12-17. http://www.interniche.org/ug/studies/tudent-assessment-educational-benefits-prepubertal-gonadectomy-program-preliminary-findings

Ille, N., Aurich, C. and Aurich, J. (2016). Physiological stress responses of mares to gynecologic examination in veterinary medicine. J Equine Vet Sci 43, 6-11. doi:10.1016/j.jevs.2016.04.010

Jaskowski, J. M., Sobolewski, J., Wieczorkiewicz, M. et al. (2020). Modern techniques of teaching bovine rectal palpation: opportunities, benefits and disadvantages of new educational devices. Medycyna Weterynaryjna-Veterinary Medicine-Science and Practice 76, 5-10. doi:10.21521/mw.6324

Jensen, K. K. (2017). How should death be taken into account in welfare assessments? J Agric Environ Ethics 30, 615-623. doi:10.1007/s10806-017-9688-1

Jukes, N. (2004). Are animals necessary in biological education? ATLA 32, 753-754. doi:10.1177/026119290403201s124

Kaldewaij, F. (2006). Animals and the Harm of Death. In M. Kaiser and M. E. Lien (eds.), Ethics and the Politics of Food. Oslo, Norway: Congress of the European Society for Agricultural and Food Ethics.

Kinnison, T., Forrest, N. D., Frean, S. P. et al. (2009). Teaching bovine abdominal anatomy: use of a haptic simulator. Anatomical Sciences Education 2, 280-285. doi:10.1002/ase.109

Knight, A. (2007). The effectiveness of humane teaching methods in veterinary education. ALTEX 24, 91-109. doi:10.14573/altex.2007.2.91

Knight, A. (2011). The Costs and Benefits of Animal Experiments. The Palgrave Macmillan Animal Ethics Series. London, UK: Palgrave Macmillan UK.

Knight, A. (2012). The potential of humane teaching methods within veterinary and other biomedical education. ALTEX Proceedings 1, 365-375. doi:10.14573/altex.2007.2.91

Kovatch, K. J., Powell, A. R., Green, K. et al. (2020). Development and multidisciplinary preliminary validation of a 3-dimensional-printed pediatric airway model for emergency airway front-of-neck access procedures. Anesth Analg 130, 445-451. doi:10.1213/ane.0000000000003774

Kuhse, H. and Singer, P. (1998). A Companion to Bioethics. Malden, MA, USA: Blackwell Publishing.

Labrague, L. J., McEnroe-Petitte, D. M., Bowling, A. M. et al. (2019). High-fidelity simulation and nursing students' anxiety and self-confidence: a systematic review. Nurs Forum 54, 358-368. doi:10.1111/nuf.12337

Lewis, J. L. (2015). A comparison between two different activities for teaching learning principles: virtual animal labs versus human demonstrations. Scholarship of Teaching and Learning in Psychology 1, 182. doi:10.1037/stl0000013

Marker, S., Mohr, M. and Østergaard, D. (2019). Simulation-based training of junior doctors in handling critically ill patients facilitates the transition to clinical practice: an interview study. BMC Med Educ 19, 11. doi:10.1186/s12909-018-1447-0

Martinsen, S. and Jukes, N. (2005). Towards a humane veterinary education. J Vet Med Educ 32, 454-460. doi:10.3138/jvme.32.4.454

McLaughlin, C., Barry, W., Barin, E. et al. (2019). Multidisciplinary simulation-based team training for trauma resuscitation: a scoping review. J Surg Educ 76, 1669-1680. doi:10.1016/j.jsurg.2019.05.002

Meurling, L., Hedman, L., Sandahl, C. et al. (2013). Systematic simulation-based team training in a Swedish intensive care unit: a diverse response among critical care professions. BMJ Quality and Safety 22, 485-494. doi:10.1136/bmjqs-2012-000994

Moher, D., Liberati, A., Tetzlaff, J. et al. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6, e1000097. doi:10.1371/journal.pmed.1000097

Müller, L. R., Tipold, A., Ehlers, J. P. et al. (2019). TiHoVideos: veterinary students' utilization of instructional videos on clinical skills. BMC Vet Res 15, 326. doi:10.1186/s12917-019-2079-2

Nakao, T., Sato, T., Moriyoshi, M. et al. (1994). Plasma cortisol response in dairy cows to vaginoscopy, genital palpation per rectum and artificial insemination. Journal of Veterinary Medicine Series A - Physiology Pathology Clinical Medicine 41, 16-21. doi:10.1111/j.1439-0442.1994.tb00060.x

Oakley, J. (2012). Science teachers and the dissection debate: perspectives on animal dissection and alternatives. International Journal of Environmental and Science Education 7, 253-267. doi:10.1080/21548455.2016.1254358

Oakley, J. (2013). "I didn't feel right about animal dissection". Dissection objectors share their science class experiences. Society & Animals 21, 360-378. doi:10.1163/15685306-12341267

Oberoi, G., Eberspächer-Schweda, M. C., Hatamikia, S. et al. (2020). 3D printed biomimetic rabbit airway simulation model for nasotracheal intubation training. Frontiers in Veterinary Science 7, 587524. doi:10.3389/fvets.2020.587524

Okhovat, S., Milner, T. D., Clement, W. A. et al. (2020). Validation of animal models for simulation training in pediatric laryngotracheal reconstruction. Ann Otol Rhinol Laryngol 129, 46-54. doi:10.1177/0003489419870820

Patronek, G. J. and Rauch, A. (2007). Systematic review of comparative studies examining alternatives to the harmful use of animals in biomedical education. J Am Vet Med Assoc 230, 37-43. doi:10.2460/javma.230.1.37

Paul, E. S. and Podberscek, A. L. (2000). Veterinary education and students' attitudes towards animal welfare. Vet Rec 146, 269-272. doi:10.1136/vr.146.10.269

Pawlowski, J. B., Feinstein, D. M. and Gala, S. G. (2018). Developments in the transition from animal use to simulation-based biomedical education. Simulation in Healthcare 13, 420-426. doi:10.1097/sih.0000000000000310

Pereira, G. D., Dieguez, J., Demirbas, Y. S. et al. (2017). Alternatives to animal use in veterinary education: a growing debate. Ankara Universitesi Veteriner Fakultesi Dergisi 64, 235-239. doi:10.1501/Vetfak_0000002804

Pirrone, F., Mariti, C., Gazzano, A. et al. (2019). Attitudes toward animals and their welfare among Italian veterinary students. Veterinary Sciences 6, 19. doi:10.3390/vetsci6010019

Quilici, A. P., Bicudo, A. M., Gianotto-Oliveira, R. et al. (2015). Faculty perceptions of simulation programs in healthcare education. International Journal of Medical Education 6, 166-171. doi:10.5116/ijme.5641.0dc7

Quiroga, M. d. M., Clarke, S. and Rajan, R. (2016). Online simulations to support the teaching of physiology. FASEB J 30, 553.521. doi:10.1096/fasebj.30.1_supplement.553.21

Rathod, S., Ghoderao, D., Kolte, V. et al. (2019). Simulation-based surgical skill training in internship program. SRM Journal of Research in Dental Sciences 10, 135. doi:10.4103/srmjrds.srmjrds_45_19

Rezende-Filho, F. M., da Fonseca, L. J. S., Nunes-Souza, V. et al. (2014). A student-centered approach for developing active learning: the construction of physical models as a teaching tool in medical physiology. BMC Med Educ 14, 189. doi:10.1186/1472-6920-14-189

Richardson, E. F., Gregory, C. R. and Sucre, E. (1994). Enhancement of the surgical education of fourth year veterinary students by participation in juvenile ovariohysterectomy and castration program. Vet Surg 23, 415. doi:10.1111/j.1532-950X.1994.tb00500.x

Rosen, M. A., Weaver, S. J., Lazzara, E. H. et al. (2010). Tools for evaluating team performance in simulation-based training. Journal of Emergencies, Trauma and Shock 3, 353-359. doi:10.4103/0974-2700.70746

Rubeis, G. and Steger, F. (2018). Is live-tissue training ethically justified? An evidence-based ethical analysis. ATLA 46, 65-71. doi:10.1177/026119291804600206

Russell, W. M. S. and Burch, R. L. (1959). The Principles of Humane Experimental Technique. London, UK: Methuen.

Salas, E., Rosen, M. A., Held, J. D. et al. (2009). Performance measurement in simulation-based training: a review and best practices. Simulation & Gaming 40, 328-376. doi:10.1177/1046878108326734

Self, D. J., Schrader, D. E., Baldwin, J. D. et al. (1991). Study of the influence of veterinary medical education on the moral development of veterinary students. J Am Vet Med Assoc 198, 782-787. https://europepmc.org/article/med/1953847

Silverplats, K., Jonsson, A. and Lundberg, L. (2016). A hybrid simulator model for the control of catastrophic external junctional haemorrhage in the military environment. Advances in Simulation 1, 5. doi:10.1186/s41077-016-0008-z

Strittmatter, S. (2017). Undervaluation of suffering of experimental animals in Germany. ALTEX 34, 435-438.

Šilar, J., Polák, D., Mládek, A. et al. (2019). Development of in-browser simulators for medical education: introduction of a novel software toolchain. J Med Internet Res 21, e14160. doi:10.2196/14160

Tanya, S. and Dubrowski, A. (2020). Development of a cost-effective pediatric intubation task trainer for rural medical education. Cureus 12, e6604. doi:10.7759/cureus.6604

Taylor, K., Rego, L. and Weber, T. (2018). Recommendations to improve the EU non-technical summaries of animal experiments. ALTEX 35, 193-210. doi:10.14573/altex.1708111

Tolbert, S. (2019). Queering dissection: “I wanted to bury its heart, at least”. In C. Taylor, C. Amade-Escote and A. Abbas (eds.), Gender in Learning and Teaching: Feminist Dialogues Across International Boundaries. London, UK: Routledge.

Ulmer, F., Lennertz, J., Greif, R. et al. (2020). Emergency front of neck access in children: a new learning approach in a rabbit model. Br J Anaesth 125, e61-e68. doi:10.1016/j.bja.2019.11.002

Valliyate, M., Robinson, N. G. and Goodman, J. R. (2012). Current concepts in simulation and other alternatives for veterinary education: a review. Vet Med (Praha) 57, 325-337. doi:10.17221/6261-vetmed

van Vollenhoven, E., Fletcher, L., Page, P. C. et al. (2017). Heart rate variability in healthy, adult pony mares during transrectal palpation of the reproductive tract by veterinary students. J Equine Vet Sci 58, 68-77. doi:10.1016/j.jevs.2017.08.013

Villanueva, C., Xiong, J. and Rajput, S. (2019). Simulation‐based surgical education in cardiothoracic training. ANZ J Surg doi:10.1111/ans.15593

Vogt, L., Duckwitz, V., Arlt, S. P. et al. (2019). Teaching small animal reproduction via virtual patients. Reproduction in Domestic Animals doi:10.1111/rda.13598

Waldau, P. (2007). Veterinary education as leader: which alternatives? J Vet Med Educ 34, 605-614. doi:10.3138/jvme.34.5.605

Wijewickrema, S., Ma, X., Piromchai, P. et al. (2018). Providing Automated Real-Time Technical Feedback for Virtual Reality Based Surgical Training: Is the Simpler the Better? In C. Penstein Rosé, R. Martínez-Maldonado, H. U. Hoppe, R. Luckin, M. Mavrikis, K. Porayska-Pomsta, B. McLaren and B. du Boulay (eds.), Artificial Intelligence in Education, Lecture Notes in Computer Science. Cham: Springer International Publishing.

Xiberta, P. and Boada, I. (2019). IVET, an Interactive Veterinary Education Tool. J Anim Sci 97, 932-944. doi:10.1093/jas/sky471

Yankelevitch-Yahav, R., Franko, M., Huly, A. et al. (2015). The forced swim test as a model of depressive-like behavior. JoVE e52587. doi:10.3791/52587

Yeates, J. W. (2010). Death is a welfare issue. Journal of Agricultural and Environmental Ethics 23, 229-241. doi:10.1007/s10806-009-9199-9

Yong, J. A. A., Case, J. B., Kim, S. E. et al. (2019). Survey of instructor and student impressions of a high-fidelity model in canine ovariohysterectomy surgical training. Vet Surg 48, 975-984. doi:10.1111/vsu.13218

Zemanova, M. A. and Knight, A. (2021). The educational efficacy of humane teaching methods: a systematic review of the evidence. Animals 11, 114. doi:10.3390/ani11010114

Zuna, I. and Holt, A. (2017). ADAM, a hands-on patient simulator for teaching principles of drug disposition and compartmental pharmacokinetics. Br J Clin Pharmacol 83, 2426-2449. doi:10.1111/bcp.13357