Slov Vet Res 2023 | Vol 60 No 3 | 155 An Insight Into Veterinary Students’ Perceptions on the use of 3D-Printed Bone Biomodels in Anatomy Learning Key words veterinary anatomy education; 3D printing; bone biomodel; student perspective Alper Koçyiğit1*, Hasan Huseyin Ari2, Baris Atalay Uslu3 1Department of Reproduction and Artificial Insemination, Faculty of Veterinary Medicine, Ondokuz Mayis University, 55139, Turkey, 2Department of Anatomy, Veterinary Faculty, Kyrgyz-Turkish Manas University, Bishkek, Kyrgyzstan Republic, 3Department of Reproduction and Artificial Insemination, Faculty of Veterinary Medicine, Sivas Cumhuriyet University, 58140, Sivas, Turkey *Corresponding author: vhkalper@gmail.com Abstract: Today, conventional teaching methods are losing their effectiveness at trans- ferring knowledge and skills, prompting the presentation of alternative strategies that hold more promise. One of the innovative alternative education materials in veterinary anatomy education is the models produced on three-dimensional (3D) printers. The subject of this study is 4 different bone biomodels 3D modeled and printed with refer- ence to cadaver-derived bones. In the study, a total of 298 students were asked to evalu- ate these biomodels in terms of their similarity to the reference bones. According to the survey, 75.5% of the students stated that their biomodel resembled the reference bones. In addition, 64.8% of these students stated that the use of biomodels can be efficient in learning the skeletal system. These outcomes showed that a sample from each of the 4 main bone types could be replicated on a 3D printer with an acceptable similarity ratio. Based on student opinions about these four different biomodels, we think that 3d printed biomodels deserve to be evaluated as an alternative in anatomy education. Received: 18 January 2023 Accepted: 5 July 2023 DOI 10.26873/SVR-1686-2023 UDC 636.09:614.253.4:591.4:612.75:159.953.5 Pages: 155–60 Original Research Article Introduction It is commonly admitted that anatomy education is a very significant field in both human and veterinary medicine (1). The main purpose of anatomy education is to provide students with required basic information of the field via effective learning and teaching methods (2). In theoretical and practical anatomy classes, methods such as verbal expression, visual expression (e.g., slide shows, training videos), software containing 3D visuals, virtual reality, and augmented reality, are widely utilized (3-5). Besides the mentioned methods, educational materials such as cadavers are utilized in practical anatomy education to increase the quality of the training. Plaster, clay, or plastic models, and plastinates, which are acquired from cadavers, are also of use (6-8). While the computer simulations or atlas pictures, which are used in anatomy training, appeal only to the visual attention of the students, plastinates, clay or plastic models, and cadavers attract visual attention and provide a tactile experience. Educational materials, which are procured from cadavers, provide students with the opportunity to know actual anatomical variations as well as get visual and tactile information (9). Besides the ethical concerns, supplying the educational materials from dead organisms is difficult and the amount of the material is generally inadequate. Furthermore, smell, texture, and students’ awareness about the fact that the materials are procured from dead organisms, cause a significant degree of motivational decrease in the learning process/success of the students. One of the innovative alternative educational materials in applied anatomy education is the models produced on three- dimensional printers. Three-dimensional printers, which are regarded as future technology, offer various advantages in terms of material production by going beyond conventional manufacturing methods. 3D printing is defined as the physical output of a 3D design. It is considered different from the conventional production methods which are based on cutting, punching, and molding. These models 156 | Slov Vet Res 2023 | Vol 60 No 3 are claimed to become realistic alternatives of educational materials in comparison with the both conventional models and cadavers (10-12). The use of 3D printers and adaptation of the 3D outputs in anatomy training is an up-to-date and original subject that is still being studied (13-15). In our study, 4 different biomodels were produced based on cadaver-derived bones. The biomodels were presented to the students for review along with the bones. Students were asked to compare the similarity of biomodels with cadaver bones. In this study, it was aimed to investigate the potential of biomodels as an alternative educational tool by using the student’s point of view. Materials and methods Reference materials of the study were obtained from the bone archive of Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Anatomy Department. All stages of biomodel production of reference bones were carried out in the Biomodel Laboratory of Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Andrology Department. The method of the study includes the stages of preparing reference bones, 3D modeling and processing of data sets, printing the biomodel on a 3D printer, and statistical evaluation of the models. Preparing samples For the production of biomodels, equidea humerus was selected as the sample of long bones; equidae ossa coxae was selected as the sample of flat bones; an equidea 3rd phalanx was selected as the sample of short bones; and finally, an equidea 3rd cervical vertebra was selected as sample of irregular bones. Using these cadaver-derived reference bones, 3D bone biomodels were produced through replication. 3D modeling and processing data sets Optical scanning method was utilized to obtain 3D volu- metric data of each selected bone. Upon placing the ref- erence bones on the scanning bench, datasets of 0.5mm precision were obtained from the bones which were 360° scanned continuously via a 3D scanner (Structure Sensor, Occipital Inc, USA). The object file format (.obj) data sets were transferred to the computer. The initial analysis of the data sets was carried out via modeling software (3D Builder, Microsoft Corporation) and unnecessary details were eliminated. Upon completing the initial analysis, the evaluation of the data sets was carried out via the com- puterized 3D graphics software (ZBrush, Pixologic). Thanks to this software, geometrical deviations, which stem from the 3D scanning process, were controlled. Biomodels were visually compared with reference bones in terms of their similarities/differences. The redundant data points were Figure 1: Appearance of specimens with flat and short bones. a; coxae digital model b; coxae biomodel c; 3rd phalanx digital model d; 3rd phalanx biomodel Figure 2: Appearance of specimens with long bones. a; humerus digital model b; humerus biomodel Figure 3: Appearance of specimens with irregular bones. a; 3rd cervical vertebra digital model b; 3rd cervical vertebra biomodel Slov Vet Res 2023 | Vol 60 No 3 | 157 removed and a single continuous mesh was created. 3D models and reference bones were compared by the anato- mist. It was checked whether the 3D printed models had im- portant anatomical features as in the bone from which they were referenced. For the similarity control of the biomodels, 8 criteria for humerus, 7 for coxae, 5 for phalanx and 5 for vertebra were considered. Incomplete-insufficient parts on the 3D models have been edited (e.g. smoothing of facies articularis in the phalanx model). To convert the complete data sets to 3D printing compatible format (gcode). The data sets were transferred to the rendering software (idea- Maker 4.0.1, Raise 3D Technologies, Inc.) of the 3D printer. 3D printing Rendered data sets were transferred to the 3D printer (Raise 3D N2 Plus, Raise, USA). For the 3D printing process, previously tested and approved poly-lactic acid (PLA) filament (nGen, Colorfabb) was used (Figure 1,2,3). The printing parameters were selected as layer height of 0.28 mm and printing speed of 40 mm/s. Gathering data The data of the study was gathered via a quantitative descriptive method. For this purpose, a total of 298 students, who took the Anatomy course of Sivas Cumhuriyet University, Faculty of Veterinary Medicine, were included in the study without sampling. In the faculty where the study was carried out, anatomy course is taught as a total of 12 hours, 4 hours of which is theoretical lectures and 8 hours are practical lectures. While textbooks and atlases are used in the theoretical part of the course, cadavers and plastic models are used in the practical part. The reference bones and biomodels were given to the participants and the participants were asked to examine both groups of materials. Following this step, a Likert scale survey, which measures the attitude of the students towards applied anatomy class and used materials, was filled by the participants (Appendix 1). Evaluation of the data and statistical analysis The data obtained from the students were analyzed using SPSS Statistics v.23 for Windows. The students were asked to choose the most suitable one among these options. For the positive items, the options were scored on a Likert-type scale (5 = strongly agree, 4 = agree, 3 = undecided, 2 = dis- agree, 1 = strongly disagree). When interpreting the arith- metic means, it was considered that the mean values be- tween 1.00 and 1.80 were of value to the extent of strongly disagree, that those between 1.81 and 2.60 were of value to the extent of disagreeing, that those between 2.61 and 3.40 were of value to the extent of undecided, that those between 3.41 and 4.20 were of value to the extent of agree, and that those between 4.21 and 5.00 were of value to the extent of strongly agree. Proportional data were analyzed by using the chi-square test. The method for collecting and evaluating data was designed as double-blind. Research ethics committee approval For the study, required approvals were obtained from Sivas Cumhuriyet University Non-Invasive Clinical Research Ethics committee (Res. Number: 2018/10-20) Results In the study, a survey was applied to a total of 298 participants, 108 of whom were female and 190 of whom were male. In this survey, the participants’ opinions about practical anatomy class, used class materials, and use of biomodels were gathered. When the students’ responses for the statements in the attitude scale were evaluated, it became clear that only 21.2% of the participants found the practical anatomy classes adequate (Table 1). On the other hand, 49.7% of the participants stated that they are disturbed by the smell when they use bones in practical classes (Table 2). In the attitude scale, when the feedback given by the participants to the statements about the use of bio-models is examined, the rate of the participants who find biomodels similar to bones appears to be 75.5% (Table 3). In addition to these, the rate of the participants who find the use of biomodels beneficial in learning the skeletal system is 64.8% (Table 4). According to the feedback given for the statement, for which the participants were asked to rate the materials in the applied anatomy classes according to their efficiency levels, it was observed that the most efficient material after the bones is the biomodel (Figure 4). Table 1: Distribution of the feedback for the statement “Practical classes are adequate” n % Strongly disagree 42 14.1 Disagree 75 25.2 Partly agree 118 39.6 Agree 53 17.8 Strongly agree 10 3.4 Total 298 100 Mean: 2.71 , Std. Deviation: 1.02. 158 | Slov Vet Res 2023 | Vol 60 No 3 Discussion The success level of veterinarians in their professional life depends on learning skills in many practical fields during their education/training. Anatomy class is the basis of the long training process leading to veterinary medicine (16). In veterinary faculties, students are first faced with the anatomy course. Knowledge of anatomy is acquired with considerable difficulty. In anatomy education, in addition to the quality of the theoretical courses in veterinary faculties, the education standards of practical classes are also tried to be increased and enriched to overcome the educational difficulties (17). The preparation of cadaver poses a variety of challenges, including ethical dilemmas, moral concerns, and complications known as the dissection experience. The development of students clinical skills is directly related to the diversity of the mentioned educational materials. However, obtaining these materials is significantly challenging in financial, ethical, legal, and cultural terms (18, 19). Furthermore, these bones must be processed with a series of chemical solutions to be able to make the bones available for the use of students (20). Formaldehyde and other chemicals, which are the components of these solutions, pose a significant level of threat to the health of both students and trainers (21). Due to the possible hazards of the chemicals which are used in the preparation of practice materials, the use of cadavers is restricted by legal regulations (22). It was determined that only 21.2% of the students find the applied anatomy lessons sufficient in this study when the opinions of the participants to the statements were evaluated on the attitude scale. However, encountering cadavers and bones in the anatomy class causes concerns with the students. Furthermore, this situation leads some students to avoid or to skip practical classes (23, 24). This outcome is not confusing, because the reason for preferring veterinary faculty is undoubtedly the love of animals and the desire to help them for many students. Table 2: Distribution of Participants’ Feedback for the Statements about Bone Use (%) Statements Strongly Disagree Disagree Partly Agree Agree Strongly Agree Mean Std. Deviation Disturbed by the smell of bone. 11.1 18.1 21.1 26.2 23.5 3.32 1.31 Disturbed by the texture of bone. 24.2 33.2 25.2 9.1 8.4 2.44 1.19 Disturbed by bones’ belonging to a dead animal. 45.6 30.2 12.8 6.0 5.4 1.95 1.14 Table 3: Distribution of Participants’ Feedback for the Statements about Biomodel Use (%) Statements Strongly Disagree Disagree Partly Agree Agree Strongly Agree Mean Std. Deviation Can distinguish the species on biomodels. 3.4 7.0 23.2 45.3 20.8 3.73 0.97 Biomodels resemble the bones. 3.7 2.3 18.1 46.6 28.9 3.94 0.94 Table 4: Distribution of Participants’ Feedback to the Statement “Utilizing biomodels in learning skeletal system is efficient” n % Strongly disagree 21 7,0 Disagree 20 6.7 Partly agree 63 21.1 Agree 89 29.9 Strongly agree 104 34.9 Total 298 100 Mean: 3.79 , Std. Deviation: 1.19. Figure 4: Distribution of the average of utility rating of educational materials according to student attitudes (1: Useless – 5: Very Useful) Slov Vet Res 2023 | Vol 60 No 3 | 159 While anatomy education requires as many samples and varieties of bones as possible, it is also under pressure of perspectives and regulations which prioritize animal welfare. Many anatomy trainers still believe that the ideal form of anatomy education can be provided only through classic cadaver-bone samples which are prepared via methods that have been practiced for longer than a century. However, the search for an alternative method to animal use for educational purposes has become a rising perspective (25, 26). Alternative educational tools such as dummies and models have begun to be utilized in basic classes like Morphology and Andrology (4, 27). Until recently, the inadequate details of these models were a major problem for this field. Biomodels present a novel option for advancing the field of veterinary anatomy education. In this study, the ratio of participants, who perceive the biomodels successful in terms of resembling the reference bones, appears to be 75.5%. In addition, the ability to recognize animal species from bone samples has been demonstrated with high success (79.5%) by the students participating in this study. This showed us that the replication of the reference bones was achieved at a sufficient level. The high-level resemblance of biomodels to reference bones can contribute to the motivation and learning success of students. On the other hand, considering that 49.7% of the participants are disturbed by the smell while using bones in practical classes, the advantage of utilizing biomodel stands out even further. Kucukaslan et. al. reported that the students are particularly hesitant in touching pig, cat, and dog cadavers (28). The fact that the biomodels are similar to the ones and not taken from live animals increases the motivation of students to learn by touching. In another study stated the idea that animal use in biomedical studies is essential (29). This idea is supported by the results of another study, which claims that the most effective learning material is bone. In that study, 28.4% of the participants claimed that personal notes such as sketches are the best learning tools for anatomy class, and 23.7% of them stated that they found the use of textbooks useful, while 14.4% of the participants regarded the anatomy atlas as the best option. Moreover, the ratio of the participants who found plastic models efficient was only 5.4%. In this study, biomodels were interestingly found to be more effective than textbooks and anatomy atlas, and biomodels were stated as the second most useful tool after bone. This outcome stems from the utilization of innovative materials and technologies. Participants adopting such an attitude supports the literature perspective which states that the transfer of knowledge through biomodels will help in clinic practice (1, 17). Thanks to the 3D printers; production costs will be reduced, and it will be possible to provide each student with an individual biomodel. In addition to the mentioned advantages of biomodels, it must also be remembered that biomodels can also be utilized in other classes such as Pathology, Surgery, Radiology, and Reproduction. However, the utilization of biomodels in anatomy training also has some limitations and disadvantages. The experience gained from dissection practice and necropsy training cannot be substituted adequately by these biomodels (30). The creation of biomodel collections for a variety of animal species within veterinary science will require a significant amount of time. The inability to model small structures (bones of the middle ear) and to maintain color harmony are the main limitations. However, studies on 3D modeling and printing of these structures continue (31). It is predicted that developments will be achieved in this field parallel to the developments in imaging and image processing technologies. Conclusion As a result, in our current environment, in which science and technology are developing rapidly, the transfer of knowledge and skills via traditional teaching methods is also losing its validity and plausible alternative strategies are put forward. The use of biomodels should be considered as an alternative that can increase the efficiency of the training process in veterinary medicine. Furthermore, the use of biomodels in practical classes can be of help in relieving the anxiety and discomfort of students. In this study, it has been shown that biomodel replicas from 4 different cadaver bones can be produced with an innovative method, each with its own anatomical criteria. Moreover, it was concluded that the students deemed these biomodels remarkably alike to their references and approved of their implementation. We think that diversifying education with alternative learning tools will benefit all stakeholders of veterinary medicine, especially students. Acknowledgements The authors declared that there is no conflict of interest. References 1. McLachlan JC, Bligh J, Bradley P, Searle J. Teaching anatomy without cadavers. Med Educ 2004; 38: 418–24. 2. Groscurth P, Eggli P, Kapfhammer J, Rager G, Hornung JP, Fasel J. Gross anatomy in the surgical curriculum in Switzerland: improved cadaver preservation, anatomical models, and course development. Anat Rec 2001; 265: 254–6. 3. Hart LA, Wood MW, Weng H-Y. Mainstreaming alternatives in veterinary medical education: resource development and curricular reform. J Vet Med Educ 2005; 32: 473–80. 4. McMenamin PG, Quayle MR, McHenry CR, Adams JW. The production of anatomical teaching resources using three‐dimensional (3D) printing technology. Anat Sci Educ 2014; 7: 479–86. 5. Persaud TVN. Early history of human anatomy: from antiquity to the beginning of the modern era. Illinois: Charles C Thomas Publisher, 1984. 160 | Slov Vet Res 2023 | Vol 60 No 3 6. Bickley HC, Von Hagens G, Townsend F. An improved method for the preservation of teaching specimens. Arch Pathol Lab Med 1981; 105: 674–6. 7. McLachlan JC, Patten D. Anatomy teaching: ghosts of the past, present and future. Med Educ 2006; 40: 243–53. 8. Oh CS, Kim JY, Choe YH. Learning of cross‐sectional anatomy using clay models. Anat Sci Educ 2009;2:156–9. 9. Dinsmore CE, Daugherty S, Zeitz HJ. Teaching and learning gross anatomy: dissection, prosection, or “both of the above?”. Clin Anat 1999; 12: 110–4. 10. Lioufas PA, Quayle MR, Leong JC, McMenamin PG. 3D printed models of cleft palate pathology for surgical education. Plast Reconstr Surg Glob Open 2016; 4: e1029. doi: 10.1097/GOX.0000000000001029 11. Lipson H, Kurman M. Fabricated: the new world of 3D printing. Indianapolis: John Wiley & Sons, 2013. 12. Murphy S, Atala A. 3D bioprinting of tissues and organs: Nat Biotechnol 2014; 32: 773–85. 13. Kurenov SN, Ionita C, Sammons D, Demmy TL. Three-dimensional printing to facilitate anatomic study, device development, simulation, and planning in thoracic surgery. J Thorac Cardiovasc Surg 2015; 149: 973–9. 14. Li F, Liu C, Song X, Huan Y, Gao S, Jiang Z. Production of accurate skeletal models of domestic animals using three‐dimensional scanning and printing technology. Anat Sci Educ 2018; 11: 73–80. 15. Lim KHA, Loo ZY, Goldie SJ, Adams JW, McMenamin PG. Use of 3D printed models in medical education: a randomized control trial comparing 3D prints versus cadaveric materials for learning external cardiac anatomy. Anat Sci Educ 2016; 9: 213–21. 16. Guevar J. The evolution of educational technology in veterinary anatomy education. Adv Exp Med Biol 2020; 8: 13–25. 17. Demirkan AC, Akalan MA, Ozdemir V, Akosman MS, Turkmenoglu I. Investigating the effects of veterinary medicine students’ learning by using the real skeleton models on anatomy theorical and practical lessons. Kocatepe Vet J 2016; 9: 266–72. 18. Abood SK, Siegford JM. Student perceptions of an animal-welfare and ethics course taught early in the veterinary curriculum. J Vet Med Educ 2012; 39: 136–41. 19. Lairmore MD, Ilkiw J. Animals used in research and education, 1966– 2016: evolving attitudes, policies, and relationships. J Vet Med Educ 2015; 42: 425–40. 20. Allouch G. Scientific technique for skeletons preservation and preparation of anatomical models to promote veterinary anatomy. J Vet Anat 2014; 7: 133–9. 21. Ajao M, Adepoju O, Olayaki A, et al. Physical reactions of Nigerian health sciences students to formaldehyde used as cadaver preservatives. Res J Appl Sci 2011; 6: 20–4. 22. 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. Off J Eur Union 2010; L276: e33–79. https://faolex.fao.org/ docs/pdf/eur98296.pdf 23. Levine ED, Mills DS, Houpt KA. Attitudes of veterinary students at one US college toward factors relating to farm animal welfare. J Vet Med Educ 2005; 32: 481–90. 24. Main DC, Thornton P, Kerr K. Teaching animal welfare science, ethics, and law to veterinary students in the United Kingdom. J Vet Med Educ 2005; 32: 505–8. 25. Ozen R, Ozen A. Attitudes of Erciyes university students to the use of animals in research. Kafkas Univ Vet Fak Derg 2010; 16: 477–81. 26. Pereira G, Dieguez J, Salgirli Demirbaş Y, Menache A. Alternatives to animal use in veterinary education: a growing debate. Ankara Univ Vet Fak Derg 2017; 64: 235–9. 27. Kocyigit A, Narlicay S. The production of testis biomodels using three‐ dimensional (3D) technologies. Andrologia 2021; 53: e14171. doi: 10.1111/and.14171 28. Küçükaslan Ö, Erdoğan S, Bulut I. Turkish undergraduate veterinary students’ attitudes to use of animals and other teaching alternatives for learning anatomy. J Vet Med Educ 2019; 46: 116–27. 29. Sugand K, Abrahams P, Khurana A. The anatomy of anatomy: a review for its modernization. Anat Sci Educ 2010; 3: 83–93. 30. Granger NA. Dissection laboratory is vital to medical gross anatomy education. Anat Rec B New Anat 2004; 281: 6–8. 31. Mennecart B, Costeur L. A Dorcatherium (mammalia, ruminantia, middle miocene) petrosal bone and the tragulid ear region. J Vertebr Paleontol 2016; 36 : e1211665. doi: 10.1080/02724634.2016.1211665 Vpogled v mnenje študentov veterine o uporabi 3D-tiskanih bioloških modelov kosti pri učenju anatomije A. Koçyiğit, H. H. Ari, B. A. Uslu Izvleček: Danes običajne metode poučevanja izgubljajo svojo učinkovitost pri prenosu znanja in spretnosti, zato bi bilo potrebno spodbujati alternativne, bolj obetavne strategije. Eno od inovativnih alternativnih učnih gradiv pri pouku veterinarske anatomije so modeli, izdelani na tridimenzionalnih (3D) tiskalnikih. Predmet te študije so štirje različni biološki modeli kosti, pripravljeni s 3D modeliranjem in tiskanjem, osnovani na kosteh, pridobljenih iz trupel. V študiji je bilo skupaj 298 študentov naprošenih, da ocenijo te biološke modele glede na njihovo podobnost s pravimi kostmi. 75,5 % študentov je navedlo, da je njihov biološki model podoben referenčnim kostem. Poleg tega je 64,8 % teh študentov izjavilo, da je uporaba bioloških modelov lahko učinkovita pri učenju skeletnega sistema. Ti rezultati so pokazali, da je mogoče vsakega od 4 glavnih tipov kosti kopirati na 3D-tiskalniku s sprejemljivim razmerjem podobnosti. Na podlagi mnenj študentov o teh štirih različnih bioloških modelih menimo, da bi 3D-tiskani biološki modeli lahko bili vrednoteni kot alternativni pripomoček pri izobraževalnem procesu anatomije. Ključne besede: poučevanje anatomije v veterini; 3D tiskanje; biološki model kosti; perspektiva študentov