Neuroanatomy, the Achille’s Heel of Medical Students. A Systematic Analysis of Educational Strategies for the Teaching of Neuroanatomy
Corresponding Author
Maria Alessandra Sotgiu
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Correspondence to: Dr. Maria Alessandra Sotgiu, Department of Biomedical Sciences, University of Sassari, viale San Pietro 43/B, 07100 Sassari, Italy. E-mail: [email protected]
Search for more papers by this authorVittorio Mazzarello
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorPasquale Bandiera
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorRoberto Madeddu
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorAndrea Montella
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorBernard Moxham
Cardiff School of Biosciences, Cardiff University, Cardiff, United Kingdom
Search for more papers by this authorCorresponding Author
Maria Alessandra Sotgiu
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Correspondence to: Dr. Maria Alessandra Sotgiu, Department of Biomedical Sciences, University of Sassari, viale San Pietro 43/B, 07100 Sassari, Italy. E-mail: [email protected]
Search for more papers by this authorVittorio Mazzarello
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorPasquale Bandiera
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorRoberto Madeddu
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorAndrea Montella
Department of Biomedical Sciences, Faculty of Medicine and Surgery, University of Sassari, Sassari, Italy
Search for more papers by this authorBernard Moxham
Cardiff School of Biosciences, Cardiff University, Cardiff, United Kingdom
Search for more papers by this authorAbstract
Neuroanatomy has been deemed crucial for clinical neurosciences. It has been one of the most challenging parts of the anatomical curriculum and is one of the causes of “neurophobia,” whose main implication is a negative influence on the choice of neurology in the near future. In the last decades, several educational strategies have been identified to improve the skills of students and to promote a deep learning. The aim of this study was to systematically review the literature to identify the most effective method/s to teach human neuroanatomy. The search was restricted to publications written in English language and to articles describing teaching tools in undergraduate medical courses from January 2006 through December 2017. The primary outcome was the observation of improvement of anatomical knowledge in undergraduate medical students. Secondary outcomes were the amelioration of long-term retention knowledge and the grade of satisfaction of students. Among 18 selected studies, 44.4% have used three-dimensional (3D) teaching tools, 16.6% near peer teaching tool, 5.55% flipped classroom tool, 5.55% applied neuroanatomy elective course, 5.55% equivalence-based instruction-rote learning, 5.55% mobile augmented reality, 5.55% inquiry-based clinical case, 5.55% cadaver dissection, and 5.55% Twitter. The high in-between study heterogeneity was the main issue to identify the most helpful teaching tool to improve neuroanatomical knowledge among medical students. Data from this study suggest that a combination of multiple pedagogical resources seems to be the more advantageous for teaching neuroanatomy.
Literature Cited
- Abulaban AA, Obeid TH, Algahtani HA, Kojan SM, Al-Khathaami AM, Abulaban AA, Bokhari MF, Merdad AA, Radi SA. 2015. Neurophobia among medical students. Neurosciences (Riyadh) 20: 37–40.
- Abushouk AI, Duc NM. 2016. Curing neurophobia in medical schools: Evidence-based strategies. Med Educ Online 21: 32476.
- Akle V, Peña-Silva RA, Valencia DM, Rincón-Perez CW. 2018. Validation of clay modeling as a learning tool for the periventricular structures of the human brain. Anat Sci Educ 11: 137–145.
- Allen LK, Eagleson R, de Ribaupierre S. 2016. Evaluation of an online three-dimensional interactive resource for undergraduate neuroanatomy education. Anat Sci Educ 9: 431–439.
- Arantes M, Barbosa JM, Ferreira MA. 2017. Neuroanatomy education: The impact on perceptions, attitudes, and knowledge of an intensive course on general practice residents. Anat Sci Educ 10: 465–474.
- Arráez-Aybar LA, Sánchez-Montesinos I, Mirapeix RM, Mompeo-Corredera B, Sañudo-Tejero JR. 2010. Relevance of human anatomy in daily clinical practice. Ann Anat 192: 341–348.
- Azer SA, Eizenberg N. 2007. Do we need dissection in an integrated problem-based learning medical course? Perceptions of first- and second-year students. Surg Radiol Anat 29: 173–180.
- Baskaran V, Štrkalj G, Štrkalj M, Di Ieva A. 2016. Current applications and future perspectives of the use of 3D printing in anatomical training and neurosurgery. Front Neuroanat 10: 69.
- Bay BH, Ling EA. 2007. Teaching of anatomy in the new millennium. Singapore Med J 48: 182–183.
- Bergman EM, van der Vleuten CP, Scherpbier AJ. 2011. Why don’t they know enough about anatomy? A narrative review. Med Teach 33: 403–409.
- Biasutto SN, Caussa LI, Criado del Río LE. 2006. Teaching anatomy: Cadavers vs. computers? Ann Anat 188: 187–190.
- Billinghurst M. 2002. Augmented Reality in Education. 1st Ed. Seattle WA: New Horizons for Learning. 5 p.
- Billings-Gagliardi S, Mazor KM. 2009. Effects of review on medical students’ recall of different types of neuroanatomical content. Acad Med 84: S34–S37.
- Brenner E. 2014. Human body preservation—Old and new techniques. J Anat 224: 316–344.
- Carr JR. 2016. Effectiveness of pre-learning online modules in the first year medical school curriculum. University of California San Diego: San Diego, CA. Master of Science Dissertation. 87 p.
- Chariker JH, Naaz F, Pani JR. 2012. Item difficulty in the evaluation of computer-based instruction: An example from neuroanatomy. Anat Sci Educ 5: 63–75.
- Chenkin J, Lee S, Huynh T, Bandiera G. 2008. Procedures can be learned on the Web: A randomized study of ultrasound-guided vascular access training. Acad Emerg Med 15: 949–954.
- D’Eon MF. 2006. Knowledge loss of medical students on first year basic science courses at the University of Saskatchewan. BMC Med Educ 6: 5.
- Dall TM, Storm MV, Chakrabarti R, Drogan O, Keran CM, Donofrio PD, Henderson VW, Kaminski HJ, Stevens JC, Vidic TR. 2013. Supply and demand analysis of the current and future US neurology workforce. Neurology 81: 470–478.
- Dao V, Yeh PH, Vogel KS, Moore CM. 2015. Applied neuroanatomy elective to reinforce and promote engagement with neurosensory pathways using interactive and artistic activities. Anat Sci Educ 8: 166–174.
- DiLullo C, McGee P, Kriebel RM. 2011. Demystifying the Millennial student: A reassessment in measures of character and engagement in professional education. Anat Sci Educ 4: 214–226.
- Dong M, Chen G, Li J, Qin K, Ding X, Peng C, Zhou D, Lin X. 2018. Three-dimensional brain arteriovenous malformation models for clinical use and resident training. Medicine (Baltimore) 97: e9516.
- Drake RL. 1998. Anatomy education in a changing medical curriculum. Anat Rec 253: 28–31.
- Drake RL. 2002. Meeting the challenge: The future of the anatomical sciences in medical school curricula. Anat Rec 269: 68.
- Drake RL. 2014. A retrospective and prospective look at medical education in the United States: Trends shaping anatomical sciences education. J Anat 224: 256–260.
- Drake RL, McBride JM, Lachman N, Pawlina W. 2009. Medical education in the anatomical sciences: The winds of change continue to blow. Anat Sci Educ 2: 253–259.
- Estai M, Bunt S. 2016. Best teaching practices in anatomy education: A critical review. Ann Anat 208: 151–157.
- Estevez ME, Lindgren KA, Bergethon PR. 2010. A novel three-dimensional tool for teaching human neuroanatomy. Anat Sci Educ 3: 309–317.
- Evgeniou E, Loizou P. 2012. The theoretical base of e-learning and its role in surgical education. J Surg Educ 69: 665–669.
- Fitzgerald JE, White MJ, Tang SW, Maxwell-Armstrong CA, James DK. 2008. Are we teaching sufficient anatomy at medical school? The opinions of newly qualified doctors. Clin Anat 21: 718–724.
- Flanagan E, Walsh C, Tubridy N. 2007. ‘Neurophobia’—Attitudes of medical students and doctors in Ireland to neurological teaching. Eur J Neurol 14: 1109–1112.
- Fredieu JR, Kerbo J, Herron M, Klatte R, Cooke M. 2015. Anatomical models: A digital revolution. Med Sci Educ 25: 183–194.
- Garas M, Vaccarezza M, Newland G, McVay-Doornbusch K, Hasani J. 2018. 3D-printed specimens as a valuable tool in anatomy education: A pilot study. Ann Anat 219: 57–64.
- Giles J. 2010. Clinical neuroscience attachments: A student’s view of ‘neurophobia’. Clin Teach 7: 9–13.
- Goodarzi A, Monti S, Lee D, Girgis F. 2017. Effect of stereoscopic anaglyphic 3-dimensional video didactics on learning neuroanatomy. World Neurosurg 107: 35–39.
- Greenwald RR, Quitadamo IJ. 2014. A mind of their own: Using inquiry-based teaching to build critical thinking skills and intellectual engagement in an undergraduate neuroanatomy course. J Undergrad Neurosci Educ 12: A100–A106.
- Greville WJ, Dymond S, Newton PM. 2016. The student experience of applied equivalence-based instruction for neuroanatomy teaching. J Educ Eval Health Prof 13: 32.
- Hall S, Lewis M, Border S, Powell M. 2013. Near-peer teaching in clinical neuroanatomy. Clin Teach 10: 230–235.
- Hall S, Stephens J, Andrade T, Davids J, Powell M, Border S. 2014. Perceptions of junior doctors and undergraduate medical students as anatomy teachers: Investigating distance along the near-peer teaching spectrum. Anat Sci Educ 7: 242–247.
- Hall SR, Stephens JR, Seaby EG, Andrade MG, Lowry AF, Parton WJ, Smith CF, Border S. 2016. Can medical students accurately predict their learning? A study comparing perceived and actual performance in neuroanatomy. Anat Sci Educ 9: 488–495.
- Hazelton L. 2011. Changing concepts of neuroanatomy teaching in medical education. Teach Learn Med 23: 359–364.
- Hennessy CM, Kirkpatrick E, Smith CF, Border S. 2016. Social media and anatomy education: Using Twitter to enhance the student learning experience in anatomy. Anat Sci Educ 9: 505–515.
- Howe N, Strauss W. 2000. Millennials Rising: The Next Generations. 3rd Ed. New York, NY: Vintage Books. 432 p.
- Javaid MA, Chakraborty S, Cryan JF, Schellekens H, Toulouse A. 2018. Understanding neurophobia: Reasons behind impaired understanding and learning of neuroanatomy in cross-disciplinary healthcare students. Anat Sci Educ 11: 81–93.
- Javan R, Davidson D, Javan A. 2017. Nerves of steel: A low-cost method for 3D printing the cranial nerves. J Digit Imaging 30: 576–583.
- Jayakumar N, Brunckhorst O, Dasgupta P, Khan MS, Ahmed K. 2015. e-Learning in surgical education: A systematic review. J Surg Educ 72: 1145–1157.
- Johnson EO, Charchanti AV, Troupis TG. 2012. Modernization of an anatomy class: From conceptualization to implementation. A case for integrated multimodal-multidisciplinary teaching. Anat Sci Educ 5: 354–366.
- Jozefowicz RF. 1994. Neurophobia: The fear of neurology among medical students. Arch Neurol 51: 328–329.
- Kam KQ, Tan GS, Tan K, Lim EC, Koh NY, Tan NC. 2013. Neurophobia in medical students and junior doctors–Blame the GIK. Ann Acad Med Singapore 42: 559–566.
- Karakas AB, Govsa F, Ozer MA, Eraslan C. 2019. 3D brain imaging in vascular segmentation of cerebral venous sinuses. J Digit Imaging 32: 314–321.
- Kerby J, Shukur ZN, Shalhoub J. 2011. The relationships between learning outcomes and methods of teaching anatomy as perceived by medical students. Clin Anat 24: 489–497.
- Khot Z, Quinlan K, Norman GR, Wainman B. 2013. The relative effectiveness of computer-based and traditional resources for education in anatomy. Anat Sci Educ 6: 211–215.
- Kockro RA, Amaxopoulou C, Killeen T, Wagner W, Reisch R, Schwandt E, Gutenberg A, Giese A, Stofft E, Stadie AT. 2015. Stereoscopic neuroanatomy lectures using a three-dimensional virtual reality environment. Ann Anat 201: 91–98.
- Korf HW, Wicht H, Snipes RL, Timmermans JP, Paulsen F, Rune G, Baumgart-Vogt E. 2008. The dissection course—Necessary and indispensable for teaching anatomy to medical students. Ann Anat 190: 16–22.
- Küçük S, Kapakin S, Göktaş Y. 2016. Learning anatomy via mobile augmented reality: Effects on achievement and cognitive load. Anat Sci Educ 9: 411–421.
- Lim KH, Loo ZY, Goldie SJ, Adams JW, McMenamin PG. 2016. 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 9: 213–221.
- Lockspeiser TM, O’Sullivan P, Teherani A, Muller J. 2008. Understanding the experience of being taught by peers: The value of social and cognitive congruence. Adv Health Sci Educ Theory Pract 13: 361–372.
- Macchi V, Porzionato A, Stecco C, Parenti A, De Caro R. 2007. Clinical neuroanatomy module 5 years’ experience at the School of Medicine of Padova. Surg Radiol Anat 29: 261–267.
- Mateen FJ, D’Eon MF. 2008. Neuroanatomy: A single institution study of knowledge loss. Med Teach 30: 537–539.
- Matthias AT, Nagasingha P, Ranasinghe P, Gunatilake SB. 2013. Neurophobia among medical students and non-specialist doctors in Sri Lanka. BMC Med Educ 13: 164.
- McBride JM, Drake RL. 2018. National survey on anatomical sciences in medical education. Anat Sci Educ 11: 7–14.
- McCarron MO, Stevenson M, Loftus AM, McKeown P. 2014. Neurophobia among general practice trainees: The evidence, perceived causes and solutions. Clin Neurol Neurosurg 122: 124–128.
- McColgan P, McKeown PP, Selai C, Doherty-Allan R, McCarron MO. 2013. Educational interventions in neurology: A comprehensive systematic review. Eur J Neurol 20: 1006–1016.
- McHanwell S, Davies DC, Morris J, Parkin I, Whiten S, Atkinson M, Dyball R, Ockleford C, Standring S, Wilton J. 2007. A core syllabus in anatomy for medical students – Adding common sense to need to know. Eur J Anat 11: S3–S18.
- McLachlan JC, Patten D. 2006. Anatomy teaching: Ghosts of the past, present and future. Med Educ 40: 243–253.
- McMenamin PG, Quayle MR, McHenry CR, Adams JW. 2014. The production of anatomical teaching resources using three-dimensional (3D) printing technology. Anat Sci Educ 7: 479–486.
- Menken M, Munsat TL, Toole JF. 2000. The global burden of disease study: Implications for neurology. Arch Neurol 57: 418–420.
- Meriac JP, Woehr DJ, Banister C. 2010. Generational differences in work ethic: An examination of measurement equivalence across three cohorts. J Bus Psychol 25: 315–324.
- Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. J Clin Epidemiol 62: 1006–1012.
- Morton DA, Colbert-Getz JM. 2017. Measuring the impact of the flipped anatomy classroom: The importance of categorizing an assessment by Bloom’s taxonomy. Anat Sci Educ 10: 170–175.
- Moxham BJ, Moxham SA. 2007. The relationships between attitudes, course aims and teaching methods for the teaching of gross anatomy in the medical curriculum. Eur J Anat 11: S19–S30.
- Moxham BJ, Pais D. 2016. How optional should regional anatomy be in a medical course? An opinion piece. Clin Anat 29: 702–710.
- Moxham BJ, Pais D. 2017. A critique of utilitarian and instrumentalist concepts for the teaching of gross anatomy to medical and dental students: Provoking debate. Clin Anat 30: 912–921.
- Moxham BJ, Plaisant O. 2007. Perception of medical students towards the clinical relevance of anatomy. Clin Anat 20: 560–564.
- Moxham BJ, Shaw H, Crowson R, Plaisant O. 2011. The future of clinical anatomy. Eur J Anat 15: 29–46.
- Moxham BJ, Plaisant O, Smith CF, Pawlina W, McHanwell S. 2014. An approach toward the development of core syllabuses for the anatomical sciences. Anat Sci Educ 7: 302–311.
- Moxham B, Plaisant O, Pais D. 2015a. The place of neuroanatomy in the curriculum. Eur J Anat 19: 215–228.
- Moxham B, McHanwell S, Plaisant O, Pais D. 2015b. A core syllabus for the teaching of neuroanatomy to medical students. Clin Anat 28: 706–716.
- Naftulin JS, Kimchi EY, Cash SS. 2015. Streamlined, inexpensive 3D printing of the brain and skull. PLoS ONE 10: e0136198.
- Olowo-Ofayoku A, Moxham BJ. 2014. Comparisons between the attitudes of medical and dental students toward the clinical importance of gross anatomy and physiology. Clin Anat 27: 976–987.
- Pais D, Casal D, Mascarenhas-Lemos L, Barata P, Moxham BJ, Goyri-O’Neill J. 2017. Outcomes and satisfaction of two optional cadaveric dissection courses: A 3-year prospective study. Anat Sci Educ 10: 127–136.
- Pandey P, Zimitat C. 2007. Medical students’ learning of anatomy: Memorisation, understanding and visualisation. Med Educ 41: 7–14.
- Patel KM, Moxham BJ. 2006. Attitudes of professional anatomists to curricular change. Clin Anat 19: 132–1341.
- Patel KM, Moxham BJ. 2008. The relationships between learning outcomes and methods of teaching anatomy as perceived by professional anatomists. Clin Anat 21: 182–189.
- Pawlina W, Drake RL. 2013. Anatomical models: Don’t banish them from the anatomy laboratory yet. Anat Sci Educ 6: 209–210.
- Preece D, Williams SB, Lam R, Weller R. 2013. “Let’s get physical”: Advantages of a physical model over 3D computer models and textbooks in learning imaging anatomy. Anat Sci Educ 6: 216–624.
- Prensky M. 2010. Teaching Digital Natives: Partnering for Real Learning. 1st Ed. Thousand Oaks, CA: Corwin Press. 224 p.
- Pytte CL, Fienup DM. 2012. Using equivalence-based instruction to increase efficiency in teaching neuroanatomy. J Undergrad Neurosci Educ 10: A125–A131.
- Rae G, Cork RJ, Karpinski AC, Swartz WJ. 2016. The integration of brain dissection within the medical neuroscience laboratory enhances learning. Anat Sci Educ 9: 565–574.
- Ridsdale L, Massey R, Clark L. 2007. Preventing neurophobia in medical students and so future doctors. Pract Neurol 7: 116–123.
- Rizzolo LJ, Rando WC, O’Brien MK, Haims AH, Abrahams JJ, Stewart WB. 2010. Design, implementation, and evaluation of an innovative anatomy course. Anat Sci Educ 3: 109–120.
- Ruisoto P, Juanes JA, Contador I, Mayoral P, Prats-Galino A. 2012. Experimental evidence for improved neuroimaging interpretation using three-dimensional graphic models. Anat Sci Educ 5: 132–137.
- Schon F, Hart P, Fernandez C. 2002. Is clinical neurology really so difficult? J Neurol Neurosurg Psychiatry 72: 557–559.
- Sidman M. 2008. Symmetry and equivalence relations in behavior. Cognit Stud 15: 322–332.
- Smith SB, Carmichael SW, Pawlina W, Spinner RJ. 2007. Latin and Greek in gross anatomy. Clin Anat 20: 332–337.
- Smith CF, Finn GM, Stewart J, Atkinson MA, Davies DC, Dyball R, Morris J, Ockleford C, Parkin I, Standring S, Whiten S, Wilton J, McHanwell S. 2016. The Anatomical Society core regional anatomy syllabus for undergraduate medicine. J Anat 228: 15–23.
- Stepan K, Zeiger J, Hanchuk S, Del Signore A, Shrivastava R, Govindaraj S, Iloreta A. 2017. Immersive virtual reality as a teaching tool for neuroanatomy. Int Forum Allergy Rhinol 7: 1006–1013.
- Stephens S, Moxham BJ. 2016. The attitudes of medical students toward the importance of understanding classical Greek and Latin in the development of an anatomical and medical vocabulary. Clin Anat 29: 696–701.
- Stephens S, Moxham BJ. 2019. Do medical students who are multilingual have higher spatial and verbal intelligence and do they perform better in anatomy examinations? Clin Anat 32: 26–34.
- Stephens JR, Hall S, Andrade MG, Border S. 2016. Investigating the effect of distance between the teacher and learner on the student perception of a neuroanatomical near-peer teaching programme. Surg Radiol Anat 38: 1217–1223.
- Turney BW. 2007. Anatomy in a modern medical curriculum. Ann R Coll Surg Engl 89: 104–107.
- Twenge JM, Campbell WK, Carter NT. 2014. Declines in trust in others and confidence in institutions among American adults and late adolescents, 1972–2012. Psychol Sci 25: 1914–1923.
- Vaccarezza M. 2018. Best evidence of anatomy education? Insights from the most recent literature. Anat Sci Educ 11: 215–216.
- Vaccarezza M, Papa V. 2014. 3D printing: A valuable resource in human anatomy education. Anat Sci Int 90: 64–65.
- Veeramani R, Madhugiri VS, Chand P. 2015. Perception of MBBS students to “flipped class room” approach in neuroanatomy module. Anat Cell Biol 48: 138–143.
- Waterston SW, Stewart IJ. 2005. Survey of clinicians’ attitudes to the anatomical teaching and knowledge of medical students. Clin Anat 18: 380–384.
- Zinchuk AV, Flanagan EP, Tubridy NJ, Miller WA, Mcullough LD. 2010. Attitudes of US medical trainees towards neurology education: “Neurophobia”—A global issue. BMC Med Educ 10: 49.
- Zurada A, Gielecki JS, Osman N, Tubbs RS, Loukas M, Zurada-Zielińska A, Bedi N, Nowak D. 2011. The study techniques of Asian, American, and European medical students during gross anatomy and neuroanatomy courses in Poland. Surg Radiol Anat 33: 161–169.