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ANATOMICAL EDUCATION Eur. J. Anat. 21 (1): 77-91 (2017) and in the Curricula of Healthcare Courses

Bernard J. Moxham 1, Hana Brichova 2, Elpida Emmanouil-Nikoloussi 3, Andy R.M. Chirculescu 4

1Cardiff School of Biosciences, Cardiff University, Museum Avenue, Cardiff CF10 3AX, Wales, United Kingdom and Department of , St. George’s University, St George, Grenada, 2First Faculty of , Institute of and Embryology, Charles University Prague, Albertov 4, 128 01 Prague 2, Czech Republic and Second Medical Facul- ty, Institute of Histology and Embryology, Charles University Prague, V Úvalu 84, 150 00 Prague 5 , Czech Republic, 3The School of Medicine, European University Cyprus, 6 Diogenous str, 2404 Engomi, P.O.Box 22006, 1516 Nicosia, Cyprus , 4Department of Morphological Sciences, Division of Anatomy, Faculty of Medicine, C. Davila University, Bucharest, Romania

SUMMARY Key words: Anatomy – Embryology – Education – Syllabus – Medical – Dental – Healthcare Significant changes are occurring worldwide in courses for healthcare studies, including medicine INTRODUCTION and dentistry. Critical evaluation of the place, tim- ing, and content of components that can be collec- Embryology is a sub-discipline of developmental tively grouped as the anatomical sciences has that relates to life before . Teratology however yet to be adequately undertaken. Surveys (τέρατος (teratos) meaning ‘monster’ or ‘marvel’) of teaching hours for embryology in US and UK relates to abnormal development and congenital medical courses clearly demonstrate that a dra- abnormalities (i.e. morphofunctional impairments). matic decline in the importance of the subject is in Embryological studies are concerned essentially progress, in terms of both a decrease in the num- with the laws and mechanisms associated with ber of hours allocated within the medical course normal development (ontogenesis) from the stage and in relation to changes in pedagogic methodol- of the ovum until parturition and the end of intra- ogies. In this article, we draw attention to the need uterine life. Complementary studies relate to the to provide within medical and dental curricula a formation and maturation of the universally accepted terminology for embryology (gametogenesis), fertilization and fecundity, and and teratology, to develop core syllabuses and, in such phenomena as parthenogenesis, , addition to providing professional training, to follow superfecundity, superfoetation (i.e. reproductive the practice of university education in taking stu- anatomy). The term ‘general embryology’ can be dents to the frontiers of knowledge. We also dis- employed to indicate the early development of the cuss different ways of teaching and assessing em- from the ovum until the formation of the bryology and teratology, preferring to see the em- primordia of systems and organs (early organo- ployment of practical methodologies, and we high- genesis). The term ‘special embryology’ may be light problems related to the poor attitudes of stu- used to follow the development of the foetus after dents towards the perceived clinical relevance of has begun. Comparative embryolo- embryology and teratology. gy compares development across . Howev- er, other than to demonstrate consistent aspects of mammalian development, comparative embryolo- gy is rarely taught nowadays to students in Corresponding author: Professor Bernard J Moxham. Cardiff healthcare courses. School of Biosciences, Cardiff University, Museum Avenue, Embryology and teratology should play a Cardiff CF10 3AX, Wales, United Kingdom. Phone: +44 (0)29 20874031; Fax: +44 (0)29 20875964. E-mail: [email protected] Submitted: 11 October, 2016. Accepted: 8 November, 2016.

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Anatomical Education

significant part in healthcare education, in terms of tology. We will concentrate on issues that centre understanding prenatal life, of grasping how the around four areas: organization of the mature body has devel- • establishing a terminology for embryology and oped, and of providing essential information for teratology; general medical practice, and pediatrics. • defining relevance and core knowledge in Students should also have an appreciation of the embryology and teratology; genetic and environmental factors that produce • understanding the importance of university congenital malformations in order to be able to education as well as professional training; understand differences between inherited, ac- • putting the teaching of embryology and tera- quired, and so-called multifactorial malformations. tology in the correct context for the healthcare Early development also has an influence on age- professions. related diseases, not least because donor tissues might have to be screened for genetic and congen- TERMINOLOGY FOR EMBRYOLOGY AND TER- ital abnormalities. Furthermore, there is now the ATOLOGY possibility of investigating, and treating, foetuses by drugs, or intra-uterine sur- Without an internationally-accepted terminology gery. Indeed, such developments are leading to a we are not able to agree on important issues of new specialty in medicine, prenatal medicine, communication across the world and between sci- which is devoted to embryonic and foetal diseases ence and the clinic. At present, responsibility on a 1 (including abnormal development) . worldwide basis for the reviewing of terminologies Embryological research is probably one of the in the anatomical sciences resides with the Inter- most productive areas for investigation within the national Federation of Associations of Anatomists 2 anatomical sciences , contributing significantly to (IFAA) and this organisation has set up several the practical and theoretical backgrounds in life terminological groups under the auspices of the sciences and medicine. Much research these days IFAA’s Federative International Programme for is at the molecular level but we are of the opinion (FIPAT) 6. FIPAT has that healthcare disciplines must not be overly re- made rapid progress across a wide front and one ductive and should not lose sight of ‘the whole of its groups is concerned specifically with embryo- body’. Indeed, morphology is increasingly relevant logical terminology, the Terminologia Embryologi- to the development of molecular science, by plac- ca being published in 2013 7. This group was - ing the manifestations of gene expression, sig- ed by John Fraher (Ireland) with 4 advisors: Bruce nalling and the processes of cell in con- Carlsen (USA), Darrell Evans (United Kingdom 3 text, in real time, in cells and tissues . To provide and Australia) , Hans ten Donkelaar (Netherlands) , an example, integration of molecular and genomic and Christoff Viebahn (Germany) . processes within embryology is a key element for Terminologia Embryologica deals with the entire fertility treatments and also for developing in vitro human intra-uterine period up until birth and pres- therapies. ently excludes postnatal development. The first Despite the importance of embryology both clini- part of the terminology is a ‘naming of parts’ (the cally and scientifically, it often seems that, alt- early stages of embryogenesis being followed by hough many universities have within their faculty a terms related to the development of the systems). significant number of embryologists, such academ- The second part of the terminology arranges the ics are generally developmental who events chronologically and employs the Carnegie have little interest in system-based, descriptive Stages for the embryonic period. Terminologia human embryology. Nevertheless, it would be ex- Embryologica was formulated according to the pected that developmental biologists wish fervently principles set out for the development of the termi- for their students to understand the finer points of nologies for gross anatomy, histology, neuroanato- their research , and indeed a university education my, anthropology, and oral anatomy. In particular, requires that students are taken to the frontiers of Latin is central to FIPAT’s way of working – “The 4 knowledge . However, it cannot be expected that Latin term is the formal, official version. It enables undergraduate students from healthcare disci- translation into any vernacular and provides an plines requiring tuition in embryology and teratolo- exact point of intersection for communication gy can deal effectively with material that is beyond across disciplines, languages, countries, regions ‘core knowledge’. and associations” 7. Some have criticized this prin- Remarkably, while there is a vast literature con- ciple , since they argue that the use of Anglicized cerning the teaching of gross anatomy to students terms offers a better basis for translation, for publi- 5 within the healthcare professions , to date there cation of research papers and books, and for dis- has been little discussion concerning the teaching cussions at international meetings. However, of embryology and teratology. In this article, we FIPAT holds to the view that, for terminologies to intend to provoke debate as a contribution to en- remain universal, prominence should not be given suring that undergraduate students have appropri- to a language currently in use since other linguistic ate education and training in embryology and tera- communities might reject a terminology if it is con-

78 B. J. Moxham et al. strued as furthering ‘linguistic imperialism’. teratology are specialities and are not of core clini- Controversially, Terminologia Embryologica , as cal relevance. Furthermore, our impression is that, for the other FIPAT terminologies, eschews epo- even where embryology continues to be taught in nyms, despite this practice being at variance with the medical course, little information is provided usage in the clinic. There is an obvious need to about teratology. This seems to us to be an unfor- bring together the embryological terminology with tunate situation since there is now a great under- clinical usage since, without the congruence of standing of embryology within the population at scientific and clinical terminologies, there will re- large, as evidenced by the frequency of Down’s main problems for educators within the field of em- in society and an understanding by lay- bryology and teratology. Indeed, a ‘Tower of persons of trisomy, and maternal and age consid- Babel’ should not be built yet higher as a result of erations about its aetiology. In addition, if a student the various biomedical, scientific, and clinical disci- does not have a clear understanding of the main plines using different terminologies. And yet, stages of normal development, (s)he will not be recognition of some ancestors and giants of em- able to understand how malformations occur or bryology is regarded by some as a sign of respect appreciate the possible association/relationship of for their achievements and an exciting detail for multiple malformations, which might be found ei- the student who wants, or needs, an explanation ther independently or linked. We will follow up for the evolution of a concept. Furthermore, wolffi- these matters by a discussion as to how core em- an, müllerian and fallopian remain standard ele- bryological and teratological knowledge can be ments in both anatomical and clinical embryologi- defined, whether medical courses are now instru- cal terms. mentalist and have moved away from the ethos of The reader is referred to the FIPAT website for university education, and the context of teaching further information and guidance 6. the disciplines in terms of methodologies that have been, or could be, adopted within medical curricu- EMBRYOLOGY AND TERATOLOGY FOR MEDI- la. CAL STUDENTS Defining Clinical Relevance and Core Embryo- As stated by Carson 8: “Embryology as a field is logical and Teratological Knowledge in a period of unprecedented change in its The amount of available knowledge relating to knowledge base. Similarly, this is a period of great embryology and teratology is beyond the require- change in medical curricular planning .” Drake et ments to learn of the medical undergraduate. In- 9 deed, including too much in the curriculum can al. (2002, 2009, 2014 ) have published a series of 12 papers showing how the time allocated to the ana- to factual overload . Consequently, course tomical sciences in medical courses in the U.S.A. organisers and medical educational authorities has declined. For embryology, there being no data often talk about the need to teach and examine for teratology, contact hours has suffered the core knowledge, supposedly meaning that which is greatest decline of all the anatomical sciences. deemed to be most clinically relevant. However, They reported that the hours devoted to embryolo- there is as yet no internationally accepted set of gy fell by over 70% between 1955 and 2014 (from core syllabuses available for the anatomical sci- approximately 60 hours to 16 hours on average). ences, embryology included. Some medical courses reported that they devoted Several attempts have been made to provide zero hours to embryology. Within the U.K., it has core syllabuses, particularly for gross anatomy. been reported that some medical schools adopt a For example, the Anatomical Society within Great Britain and Ireland has provided a core syllabus for perfunctory approach to the teaching of embryolo- 13 gy while other schools refer only occasionally to gross anatomy and others have been developed 10 by anatomical societies in America and in the the subject or even not at all . Although data of 14 this kind do not appear to have been collected Netherlands . Nevertheless, these syllabuses elsewhere in the world, anecdotally it seems that have been developed by national bodies and are similar decreases in the time allocated to embryol- not internationally-agreed syllabuses. Furthermore, ogy have occurred. Such changes have been the there is no syllabus that specifically deals with em- result of medical schools’ shift of emphasis away bryology and teratology. The IFAA, together with from a firm grounding in the the Trans-European Pedagogic Anatomical Re- and towards basic medical training that deals pri- search Group (TEPARG) that is supported by the marily with what is perceived as being of ‘clinical European Federation for Experimental Morphology 11 (EFEM), is in the process of formulating core sylla- relevance’ . The drivers for emphasising ‘clinical 15 relevance’ seem to arise partly from social and buses using Delphi Panels to initiate the process . political needs, partly from students increasingly To date, core syllabuses in the first stages of de- wishing to engage with clinical matters at the out- velopment have been published for the gross anat- omy of the head and 16 and for neuroanato- set of their studies, and partly from trends in medi- 17 cal education. Consequently, it can appear to my . These have also been announced on the medical course organisers that embryology and IFAA website so that they become available for

79 Anatomical Education

comment and amendment by interested parties training. In addition, a core syllabus does not dic- (anatomical, scientific and clinical). At the time of tate how to teach the syllabus nor when in the cur- writing, a core syllabus relating to embryology and riculum the subject has to be taught. Nevertheless, teratology for the medical course is being devel- without an internationally-recognised syllabus to oped by the IFAA/EFEM, and it is envisaged that hand, it is not easy to combat politically the contin- this will become available early in 2017 within an uing decline of embryology and teratology in the anatomical journal and on the IFAA website. medical course 9. Even when a core syllabus is arrived at, it cannot Core syllabuses are there to help ensure con- be definitive and set ‘in tablets of stone’ and it is sistency, reliability and transparency of medical important to emphasise that core syllabuses training wherever it is undertaken. They also help should not dictate what cannot be taught within the with the drive to ensure clinical relevance. Howev- medical curriculum. Consequently, the core sylla- er, there are consequences to this essentially bus must be regularly, and frequently, reviewed ‘instrumentalist’ approach to medical education since the importance of embryology and teratology that will be touched upon when considering the is increasing with clinical progress and scientific need to maintain medicinal training within a univer- advancement. Indeed, it is recognised that the in- sity setting. There are also conceptual problems put of clinicians into the development of an IFAA/ relating to defining core elements within a medical EFEM core syllabus is essential so that they guide course 18 . Presently, it seems that each medical both the scientific and clinical aspects of has its own version of what is a core sylla-

Table 1a.

THE PRE-EMBRYONIC AND EMBRYONIC PERIODS Gametogenesis, mitotic and meiotic divisions, hormones, normal /defective development of gametes, meiotic disturbance is result- ing in chromosomal aberrations; genetic regulation of formation; Maternal advanced age: nondisjunction of chromosomes, presence of chromosomal abnormalities; paternal old age: occurrence of new ; Fertilization (natural, strategies of IVF, ART); Contraceptive techniques / risks; Principles of / dysmorphogenesis, signalling pathways, cell-cell interactions; cascades of signals determine cells fate; , -mitotic division, , early formation, , primordial germ cells, genetic regulation of PGC for- mation, proliferation, migration and development, complex regulator gene cascade, , normal / defective development as a starting point of teratogenic changes, , mutations of genes cause many tumour development/ groups of cells as a basis for future tumour; Hatching, normal / pathological, assisted hatching; Chromosomal abnormalities result in spontaneous or abnormal development, 60-80% of early are lost, only 5% of implanted survive – natural screening; Dating of ; Carnegie embryo stages generally used pattern of development by weeks, months and by trimesters, periodicity of prenatal deve- lopment; Cell differentiation from totipotent cells present in the , to the pluripotent cells present in the three basic embryonic layers, sources (also cell lineage, , cell transformation); Influence of signal activity on endodermal, mesodermal and ectodermal layers differentiation; Process of establishing of the body plan and fate map of the systems and organs; , epiblast cells forming embryonic mesodermal layer, establishment of the cranio-caudal , lateralization (left-right asymmetry), dorsalization-ventralization; primi- tive node, notochordal process, basic role of signals, production of signal molecules, induction, all determinative for the formation of small groups of cells, basic „for the beginning of future development“; Formation of , , development of vesicles, and , formation of cardiogenic zone, primary and secondary plate, development and positioning of heart tube, cardiac loop; folding; coeloma differentiation, devel- opment of bases of organs of abdominal cavity and ; streams of cell, migration, (PGC, , neural crest cells etc.), , , primitive circulation; period in which differentiation of cells under the effect of failed signalling / induction results in defective development; Foetal membranes development: , buffer the embryo in the interim before the has been formed, uteropla- cental development, normal development / defects of placental development and functioning; Histology of developing embryonic ; Environmental influences: mother´s inadequate , (women living in poor conditions / lack of proteins, folic acid, vitamins), chemical pollutions, exposure to hypoxia (low level of pO2 in blood) because of mother´s and heart chronic diseases, smoking, defects of placenta; mother´s ; mother abusing (foetal alcohol syndrome) or smoking, (or both), mother abusing drugs, medicaments, infection diseases in mother viral, bacterial, parasitic, i.e. , HIV / AIDS, Zika viral infection, tuberculosis, syphilis, toxoplasmosis etc.; mental stress; physical teratogens: radiation, noise / vibrations, hyperthermia, etc.;

80 B. J. Moxham et al. bus and this certainly applies to embryology and has highlighted a dilemma in this respect, writing: teratology. Unfortunately, it seems that the core “One of the most significant questions in embryolo- syllabus often changes merely as a result of gy education for medical students is how much of changes in personnel (the medical dean, head of the ’new’ molecular embryology to mix with the department or course organiser)! This matter is ‘old’ developmental anatomy approach”. Neverthe- taken up when later we discuss the context of less, a new era of embryology was opened up. For teaching and learning the topics. What is important example, recent developments include matters to state now is that unwarranted diversity of clinical relating to fertilization and assisted reproduction training should not be accepted educationally. To beginning from gametogenesis, selection and dif- do so ultimately disadvantages both the student/ ferentiation of stem cells that raises the hope for prospective medical practitioner and the patients successful treatments of up-to-now incurable dis- by not having more universally agreed standards eases or post-traumatic lesions, ways of prevent- and syllabuses. Should governmental agencies ing stem cells producing tumours, recognition and perceive that there is not consistency, reliability understanding of the influence of teratogens (often and transparency across the sector, then they multifactorial), and study of tumour development in might impose state-wide examinations that inevita- relation to the differentiation of embryonic and foe- bly would lead to teaching that would be examina- tal structures. Such developments require careful tion-focused, and to learning that would be strate- consideration as to whether or not they are core gic according to what was assessed. This there- topics at this time, but Table 1 provides a list of fore would result in medicine moving further away topics that, even if they cannot be made available from the established university education model. in an embryological course early during medical Inevitably, a core syllabus in embryology and education, should be part of the medical curricu- teratology concentrates on descriptive topics. De- lum by the end of the medical course. scriptive embryology, while remaining as a basis of the subject matter, has been enriched by findings The Importance of a University Education in , , and electron and Consumerist societies are inevitably instrumen- scanning microscope research. Since the time talist. The Oxford Dictionary defines instrumental- when genes such as HOX , SHH , PAX were dis- ism as: “a pragmatic philosophical approach which covered, and their influence on the origin of embry- regards an activity (such as science, law, or edu- onic structures was recognized, our knowledge in cation) chiefly as an instrument or tool for some this field has been deepened. However, Carlson 19 practical purpose, rather than in more absolute or

Table 1b.

THE FOETAL PERIOD Maturation and growth of foetal organ systems; crown-rump length; processes of intensive growth, influence of biological molecules and hormones on differentiation of tissues and organs; cell proliferation; formation of ; Differentiation of definitive body topography; understanding that, although all organ systems are present by 8 weeks, few are func- tional; organs established in the embryonic period are developed to definitive positions, prepared for their function in postnatal life, a number of organs do not finish maturing until after birth; foetal movements start: differentiation of muscle proteins, muscle groups, movements, diurnal rhythm of movement originates; Microscopic anatomy and functional development of different tissues and organs; differentiation of special groups of cells important for the function of given organ; differentiation of , CNS, brain, spinal cord and PNS, and peripheral , normal and defective; sensations; cardiovascular system: this is a period of frequent development of heart defects, heart beats from forth week of pregnancy, (100 beats increasing to 150 beats per min.); endocrine glands produce small amount of hormones in- volved in foetal development: stimulates peripheral endocrine glands (i.e. activity of hormone, corticoids) ; digestive system: maturation of gastric mucosa cells that differentiate for secretory function, development of enzymes, mucosa of small intestine differentiates for process of absorption in craniocaudal direction, formation of villi followed by development of crypts 1 -2 weeks later, development of gland cells, meconium; differentiation producing small amounts of urine; lungs: alveolar lining differentiation with development of type IIpneumocytes (producer of pulmonary surfactant), note that the premature new-born lacks surfactant, giving rise to distress syndrome; placental function: hormone production continues (HCG, GRH) steroid and protein hormones and prostaglandins; differentiation of , , temporary hematopoietic organs; development of marrow tissue: hematopoietic cells are present; Critical period is when there is intensive differentiation of an organ - influence of failed signalling / failed induction or infection and toxic agents activity, and other factors causing cell modifications or mutations; teratogens reach foetus by crossing the placenta; cell changes: source of teratoma or tumour formation (tumour might be developed either in foetal period or survive perhaps for years as a ‘sleeping group of cells’ that might in future be activated to produce tumour growth; Therapy of defective organs; therapeutic manipulation on the foetus, wide range of foetal anomalies could be corrected operatively, by open foetal surgery,(e.g. hydrocephalus correction by ventriculoamniotic shunt, correction of obstructive uropathy); foetal blood transfusions; of foetus, correction of defects of development now being investigated; Delivery normal /pathological, establishing of date of delivery (usually 38 th week of pregnancy); process consists of three distinct phases of labour; role of prostaglandins F 20 ; in perinatal period: changes in lungs, new-born first inspiration with opening of the alveolar sacs, role of pulmonary surfactant; conversion of blood circulation from foetal to air- breathing pattern so that there are two circuits (pulmonary and systemic);

81 Anatomical Education

ideal terms”. In other words, the ‘truth’ of a con- prior to admission into the medical course. Howev- cept or the cultural value or history of a topic is er, these examples aside, we remain concerned regarded as of little value in the of the need to that instrumentalism in medical education could show practical worth. Instrumentalism, a relativistic mean that our medical students will be less well notion, emanated from the philosopher John Dew- versed in the scientific basis of medicine and that ey, who supposed that “thought is an instrument the trend that we see in cutting scientific courses for solving practical problems, and that truth is not will continue to the detriment of the medical profes- fixed but changes as the problems change” 20 . In sion. The previously stated decrease in the terms of medical education, this comes down to amount of time devoted to embryology in the medi- teaching clinical relevance and core topics. How- cal course is indicative of this trend 9. Within the ever, clinical relevance is often narrowly defined as United Kingdom and Ireland, it has become com- being disease-orientated, and this impoverishes monplace for many medical students to opt out of medicine by a failure to accept the functionality the medical course for a year or two to obtain an model of medicine that recognises the importance ‘intercalating’ Bachelor’s Degree, often in the bio- of normality and health 21 . Medicine might be fur- medical sciences and including a research project. ther impoverished by becoming disengaged from Indeed, options are available for students to study the standard university educational experience of aspects of embryology and teratology in this way, taking students to the frontiers of knowledge 4. although we are aware that their studies are more A problem here relates to the medical course likely to be focused upon signal molecules and being developed by a ‘top down’ approach – genetic considerations and upon experiments per- through government agencies, the medical profes- formed on Drosophila , ( Danio rerio ), sion, medical deans and/or medical educational- quail, and chick, the only popular experimental ists. Little consideration is given to the needs and being the mouse. opinions of patients/potential patients by introduc- Assuming that we persist in the notion that doc- ing ‘bottom up’ elements to course organisation tors of medicine are learned and aware of the fron- and content. This is seemingly a paradox within an tiers of knowledge so that they are prepared for increasingly consumerist society. A recent survey future scientific and medical developments, we are of laypersons’ attitudes towards the importance of of the opinion that, if the medical course is to con- gross anatomy within the medical course shows tinue to decrease the amount of time devoted to that they have a reasonable knowledge of human the biomedical sciences (including embryology and anatomy and that they strongly express the view teratology), we would encourage the medical es- that their confidence in the medical profession tablishment to think positively of maintaining (or would be greatly diminished should anatomy be introducing) intercalating medical degrees in the downgraded 22 . There is consequently a need to basic medical sciences and to include embryology develop these studies further to assess the extent and teratology in such programmes. to which laypersons have knowledge of embryolo- gy and teratology and how they view the im- The Context of Teaching Embryology and Tera- portance of these disciplines. tology No one presently is suggesting that medical Traditionally, before being placed in front of pa- schools should become separate from university tients, it was considered that students needed 2 to institutions, but the instrumentalist philosophy puts 3 years when they were informed of the scientific a strain on the relationship. In the past, medical basis of medicine. The model was thus established students received some form of university educa- that the healthy body was the first object of study, tion in the biomedical sciences prior to clinical to be subsequently followed by interpretation of training, with the student having a 2- or 3-year pre- this knowledge to appreciate how disease pro- clinical part of the medical course 5. However, this duced abnormalities. This model is exemplified by the findings in the Flexner Report in the USA model is becoming less and less recognised by 23 medical educationalists. (1910) . Within this model, embryology (rarely Perhaps this situation is related to how students teratology) would be taught as a stand-alone are recruited to the medical school. In the main, course. This would occur most often later in the worldwide, students are recruited straight from ‘preclinical’ course and after the students had secondary school and is an undergraduate learned a substantial amount of gross anatomy. In course. In some universities that recruit medical some medical schools, embryology would be inte- students straight from school, for example Oxford grated with gross anatomy, so that each discipline and Cambridge in the United Kingdom, medical would benefit from each other to the extent that the students are required to complete three years of complexities of the anatomy of the scientific training leading to a scientific degree be- could be explained by recourse to understanding fore being fully enrolled within medical schools. development. Furthermore, throughout the U.S.A., medicine is a It is also evident that teaching about malfor- postgraduate course and the students are usually mations and about teratology at an early stage of required to have undertaken a Bachelor’s Degree the medical course provides the student with early

82 B. J. Moxham et al. contact with and with clinical cases. It the medical curriculum at all 9. offers a good basis for problem-based study. As part of a survey of the attitudes of European There is also the issue of age-related diseases, medical students towards the clinical relevance of which, for the moment, lies in a sort of ‘no man’s embryology 26 , cognisance was taken of the differ- land’ and is not included in any textbook of ent arrangements for the teaching of embryology (medical) embryology. In this regard, a basic ques- in the medical schools participating. This ranged tion is: where does one stop the taught domain? from stand-alone courses to integrated teaching, Ontogenesis takes place throughout our lives, from separate departments of embryology to from fertilization until death. Other interesting, and teaching being conducted in anatomical or clinical useful, concepts deal with the embryonic vestiges, departments, and from the topics being taught by rudimentary organs, homologous and analogous specialist embryologists who are involved in devel- organs or parts of the organs. Above all, we be- opmental research to anatomists with other re- lieve that one of the important functions of an em- search or pedagogic interests. To provide exam- bryology and teratology course is to teach general ples: principles that extend beyond the detailed descrip- At a UK medical school there is not a distinct de- tive embryology present in textbooks. Indeed, we partment of embryology and the teaching of the hold that three basic concepts need to be imbed- discipline involves staff who are neither recognised ded in the embryology curriculum: experts with research experience in normal embry- 1. The relationship between and phe- ogenesis and organogenesis nor clinically quali- notype; fied. Furthermore, the teaching is scattered over 2. The concept of ‘normal’ needs to be dis- the 5 years of the medical curriculum. Indeed, cussed. It can imply the most common, the there is no longer a department of anatomy, since most functional, or even the most healthy, but this has been incorporated within a school of biolo- students need to appreciate that ‘normal anat- gy. On the other hand, at a Greek university, there omy’ is not present in ALL individuals and this is a recognized department of histology, embryolo- understanding to the third point; gy and anthropology that is distinct from a depart- 3. The continuum that exists between the ment of gross anatomy. It has stand-alone courses ‘normal’, anatomic variant, malformation, and and clinically qualified staff. Both universities, how- disability needs to be understood. It is thus ever, emphasise clinical cases that reflect on the important for medical students to understand teaching of embryology. At a Czech university, the concepts of normotype, anatomical varia- there is also a separation between the institutes of tion, heterotype, morphologic versus function- embryology (with histology) and gross anatomy, al disability, and malformation 24 , as well as while at a medical school in Romania there is a the relationship and equilibrium between gen- Laboratory of Embryology within the department of eral ontogenesis, organogenesis, histogene- Anatomy, with dedicated full-time teaching staff sis and cell transformation 25 . who are all medically qualified. They teach embry- ology for three semesters during the 1st and 2nd It is clear from the surveys of Drake et al. 9 that year of the medical course. In addition, there is an increasingly in the U.S.A. (and indeed it seems optional course on Molecular Biology of Human elsewhere in the world) the whole medical course Development for the 2nd year medical students. At is being integrated both horizontally (across a a medical school in Portugal, general and special year) and vertically (across the whole course). The embryology were taught until 2010, together with 2014 survey by Drake et al. reported that the ana- histology, in the second year of the medical curric- tomical sciences were now part of an integrated ulum, but embryology is now only taught within the curriculum in 45% of US medical courses. In rela- 5th year of the medical course and in association tion to integrated courses, there could be difficul- with paediatrics. In Malta, a short series of intro- ties relating to positioning scientific topics within ductory lectures on human development, potency, the overall medical curriculum. While there are determination, differentiation, blastogenic birth de- advantages in having scientific topics taught at a fects and stem cells is given at the start of Year 1 discreet time in the overall medical curriculum, of the course. In addition, an introductory lecture increasingly medical educationalists are thinking on the embryology of each organ system is includ- about such courses being a theme that ‘snakes’ its ed at the start of each of a series of systemic mod- way throughout the entire medical course. The ules with the topics being assessed at the end of belief is that the biomedical sciences should ap- Years 1 and 2. At a medical school in Paris, there pear throughout the medical course so that materi- is also a separation between the departments of al is delivered, not for integration within the scien- gross anatomy and embryology, and embryology tific discipline, but for providing foundation material is taught during the three first years of medical for the clinical course as and when a clinical topic school. At a medical school in Austria, there is a is taught or delivered (another aspect of instru- common department of anatomy, histology and mentalism). At the most extreme end of the spec- embryology but with a distinct ‘division’ for histolo- trum, embryology and teratology is not taught in gy and embryology with dedicated full-time staff.

83 Anatomical Education

General embryology is taught within the 2 nd term research, and setting self-study tasks with ‘wash- and further embryological and teratological as- up’ seminars can also be employed. In particular, pects in the clinical context of pregnancy are many aspects of embryogenesis and of organo- taught in the 7 th term. genesis are better understood practically by These examples demonstrate the extent of diver- means of 3D reconstructions. However, anima- sity of practice and organisation and suggest that, tions and other virtual imaging techniques (such as because of lack of appropriate pedagogic re- Digitally Reproduced Embryonic Morphology search, there are not firm foundations upon which (DREM) 29 ) are likely to be useful in enabling the to build notions of how best to teach embryology student to better appreciate the complex folding and teratology. and 3D aspects of embryology. It can therefore be argued that didactic teaching and student learning Methods of teaching embryology and teratolo- can benefit from both practical experience and gy from the use of computer imaging technologies Teaching methods appear to be as various as that improve visualization of difficult topics and those employed to teach gross anatomy. It can be embryological processes. Indeed, this is particular- envisaged that the topics could be taught simply ly necessary to explain the multifactorial relation- didactically (by lectures, tutorials, or e-learning), or ships occurring in embryology and teratology in more practically (by laboratory classes with speci- order to build embryonic/foetal ontologies and to mens, dissection and histology slides), or by correlate these with clinical malformations. Fur- means of the use of models. Furthermore, in a thermore, the use of computer imaging technolo- more integrated model, the topics can be part of gies helps the understanding of genome studies problem-based learning or problem-based teach- where regulatory variation in the embryonic/foetal ing incorporating clinical scenarios. Presently, the human genome is mapped. This is increasingly efficacies of these methods have not been ade- becoming important as we are employing quately assessed. Taking the case of problem- knowledge of the genetic factors to study epigenet- 27 based learning in general, Hattie has shown, ics and diseases such as malignant tumours that from a synthesis of 8 meta-analyses involving over are sustained by rare stem cells that originate from 38,000 subjects, that there are no beneficial edu- embryonic stem cells, and that have been affected cational effects. On the other hand, for problem- by teratogens during . In addition to new based teaching, he showed, from 6 meta-analyses computer imaging technologies, there should be involving over 15,000 persons, that there are desir- access to ultrasound techniques (if only by re- able effects. Looking at attitudes of professional course to having access to ultrasound reports), anatomists and medical students to the perceived and all teaching materials (e.g. EM (transmission value of different methodologies for teaching gross and scanning) pictures, PPT demonstrations, LM 28 anatomy , practical methods of teaching the sub- slides scans, hand drawn schemes) should be ject were preferred and theoretical methods available online to students. Furthermore, clinical (including e-learning) were not well regarded. The histories and case scenarios describing malfor- authors would hypothesise that similar findings mation development should be presented in clas- from medical students and professional embryolo- ses or during practicums. gists would also apply to the teaching of embryolo- A moot point concerns the extent to which stu- gy and teratology. dents nowadays should be taught behavioural as- However, didactic teaching approaches for stud- pects in relating to, for example, alcohol abuse and ying normal embryological/foetal development re- congenital abnormalities. Although some might main fundamental in many courses worldwide. argue that this is best left to the clinic, some Nevertheless, they are not enough to successfully acknowledgement of the issues involved should inculcate to the contemporary student all the excit- appear in an embryology and teratology course. ing and new knowledge concerning normal and Whatever pedagogic methods are used to teach abnormal embryological development, nor to teach embryology and teratology, we plead for embryolo- them about the clinical problems that arise when a gists throughout the world to collaborate through malformation is seen in a new-born who will sur- an open exchange of knowledge, using useful edu- vive despite the health problems that arise as a cational and research materials, and to work to- consequence. We would argue that new gether on pedagogic research projects to evaluate knowledge in embryology requires a new attitude what is best for teaching and for student learning to embryology teaching. For students, it is often and ultimately for the betterment of patients. hard to imagine the developmental processes oc- It can be argued that the teaching of embryology curring within the embryo. Indeed, a great number requires knowledge of the longitudinal sequence of of documents often have to be prepared for lec- events in the development of systems, organs and tures to help students visualize human develop- tissues and also appreciation of the transversal ment. 3-D reconstructions, scanning microscope correspondence between developmental aspects pictures, slides with embryological tissue sections, of systems, organs and tissues in order to under- articles outlining recent results of embryological stand the level of structural organisation step by

84 B. J. Moxham et al. step, or stage by stage. This leads us on to the Table 2. Comparisons of the chronology of events dur- thorny issue of the extent to which the learning of ing the first 23 stages of for the embryonic stages is important within the medical rat and human 30 course . Many would argue that this is not ‘core’ EMBRYONIC Rat Chronology Human Chronology knowledge but, if it is to be taught/learned, then STAGE perhaps the use of the ‘Carnegie standard stages’ 1-5 Day 1 - 7 Week 1 is best 31 . Indeed, as mentioned earlier, this is the system employed within the Terminologia Embryo- 5-6 Day 7 Week 2 logica . This system allows a better understanding 6-9 Day 7 - 9 Week 3 of the correspondence between organs and tis- 10-13 Day 9 - 11 Week 4 sues in normal development, and offers a refer- ence for understanding the potential risks of mal- 13-15 Day 11 - 12 Week 5 formations in teratology and tumour transfor- 15-17 Day 12/13 Week 6 mation. Indeed, students should appreciate that 17-19 Day 14 Week 7 each stage of development is a collection of linked events seen as a snapshot on a 4D map. If all 19-23 Day 14 - 20/21 Week 8 events belonging to a specific stage happen syn- chronously, it means that the general development offers better scientific support (see Table 2). of the body is proceeding normally, whereas, if It goes without saying that learning ALL 23 stag- some developmental events are happening earlier es would make embryology almost impossible or later, it means that the normal scheme is dis- within a course for healthcare professions, but a rupted and a malformation occurs. rational selection of the main stages that define Embryologists would hold to the opinion that significant organogenetic and histogenetic steps standard timing, measuring, featuring / defining would make it more acceptable. We advocate typical changes are essential for a correct use of therefore that the use of simplified Carnegie stag- embryology information. Of course, medical stu- es should be considered in the design of lectures dents would not be expected to know what events and student handbooks. Whether or not students are happening day by day or hour by hour, but are expected to learn the stages, it is always in- should understand the succession of events in structive for the student to be made aware of the their natural order and should appreciate that they mismatch in the timing of an event between two run in parallel within different systems, organs and different books and research articles. At the very tissues. Furthermore, they should appreciate that least, students should be made aware that using such parallel events must proceed in harmony dur- stages improves precision and avoids acquiring ing normal development, and could be unsettled contradictory data. The obverse is that, if students by teratogenic factors. merely stumble upon mistakes and contradictions, The most significant weeks in human they might come to the conclusion that reported are weeks 3 to 6/7, corresponding to stages 6 to information is not safe and that the scientific rigour 19. We note however that contemporary embryolo- of the data supplied is questionable. gy handbooks, as well as research articles, do not It should be mentioned here that the teaching of provide consistent accounts of stages and the tim- teratology is regrettably too often regarded as a ing of events. To provide a specific example from ‘Cinderella topic’, seeming to be taught perfunctori- the research of one of the authors (Chirculescu et ly or not at all. This is regrettable because of tera- al., 2010) 32 , stages 12 and 23 are key develop- tology’s importance scientifically, clinically and so- mental moments for the pituitary, and studies on cio-politically. At present, however, although there the development of the human and rat pituitary are studies on the amount of teaching of embryolo- suggest that there is discordance of timing such gy taking place in medical courses 9, there have yet that, from an assessment of when hormone posi- to be surveys undertaken on the amount of time tive immunostaining and their co-localisation in the devoted in the curriculum to teratology. We look same cells commences (in cells presumed to be forward to this anomalous situation being rectified. already differentiated), pituitary development de- There is much talk these days of introducing op- fined by weeks or by stages do not match. tionality within the medical curriculum, often as It may be regarded as unfortunate that many elective modules. The implication is that students ‘facts’ in embryology, for both normal development have a choice of courses beyond what is consid- and for the action of teratogenic agents, come ered to be core. Agarwal et al .33 have recently pro- from attempts to correlate information obtained vided a systematic evaluation of preclinical elective from human, mouse, rat, rabbit and chick. Perhaps courses in the medical curriculum and have report- we should not be surprised, since attempting to ed that “the range of electives available and their provide equivalence between a 9 month and 3 impact upon medical student education are not week gestation period is unsupportable. Neverthe- well described in the literature”. It is recognised less, drawing equivalence by considering stages that the prime purpose of such courses is to intro-

85 Anatomical Education

duce flexibility in the medical course, and to allow they are constructed together and preferably the students to follow their own individual path- taught simultaneously by embryologists and clini- ways by pursuing their own personal interests. cians. It would of course be expected that the clini- This seems to us to be a fine concept where the cian would be appreciated by the students as be- topics covered are not core. Indeed, having al- ing a specialist who has clinical cases involving ready argued that many topics in embryology and health problems associated with development of teratology should be regarded as core, we would organs and systems. However, we are concerned be dismissive of attempts to incorporate the sub- that there is a lack of medical embryologists avail- jects into optional courses or electives. Moxham able to satisfy this requirement. Moreover, in order and Pais 34 have argued that, until core material is to plead for the necessity of the survival of embry- defined (and generally agreed), then optionality ology, directors of medical education these days has conceptually no real foundation. Furthermore, frequently are looking to see not only the clinical it is worrying that the diversity of elective courses relevance of disciplines and topics, but also the (including content, teaching methodologies, as- research relevance. Accordingly, the development sessment, admissions, and outcomes) detracts of courses in human genetics and developmental from the important educational principles of con- biology can lead to a better appreciation of the sistency, reliability and transparency. Indeed, med- importance of embryology in medical education, ical education worldwide is already fractured by a and this can only be appreciated if the teaching is high degree of diversity such that there is difficulty research-led and the teachers are research-active. in appreciating the standards set (and thus the So the dilemma is finding medically-qualified, re- quality of future medical practitioners). Most con- search-active, developmental biologists who are cerning, however, is the lack of understanding of interested and capable of teaching! Perhaps this is how important embryology and teratology is to the a tall order! clinic, to patient welfare and to the concerns of society (particularly the detrimental effects of envi- The attitudes of medical students in Europe to ronmental factors and infections (viz. the Zika virus the perceived importance of embryology to the that according to teratologists will be the second clinic 35 Regardless of the methods of teaching em- most harmful teratogen after )). Thus, ployed, successful tuition in any subject depends the subjects are clearly important for obstetrics, primarily upon the enthusiasm of the teacher and paediatrics, community medicine and general the motivation of the students. In terms of motiva- practice but to provide core embryology and tera- tion, there have been many studies assessing the tology topics in an optional module before a stu- attitudes of medical students towards the per- dent has considered their future career pathway is ceived clinical relevance of the anatomical scienc- nonsensical, especially if the elective is early in the es using Thurstone and Chave’s (1951) attitude medical course (as it usually is). analyses. However, most studies have been con- In terms of who teaches embryology and teratol- cerned with reporting the attitudes towards the ogy, it can be argued that there is a need to en- clinical importance of gross anatomy 28 . For embry- sure that the teachers of embryology are clinically ology, attitudes in the early stages of their training qualified, persons with whom the students can em- of nearly 1,600 medical students studying across pathise and who can provide appropriate clinical Europe have been assessed 26 . It was reported examples. Clearly, clinical scenarios for both gross that, regardless of the university and country sur- anatomy and embryology are more powerful when veyed and also regardless of the teaching meth-

Fig. 1. Histograms comparing medical students' attitudes toward the clinical importance of gross anatomy (series 2) and for embryology (series 1) obtained using attitude analyses of Thurstone and Chave (1951). The attitude scales are from 1 (extremely positive) to 11 (extremely negative). x axis is % fre- quency; y axis is attitude scale. The data for embryology is a composite for all the countries surveyed by Moxham et al. (2016) 26 and the data for gross anatomy are taken from the paper by Moxham and Plaisant (2007) 28

86 B. J. Moxham et al. ods employed, there is significantly less under- the dental course has yet to be devised. However, standing of the importance of embryology com- in Table 3 we conjecture what such a core sylla- pared with gross anatomy. Figure 1 provides a bus might comprise and would urge the IFAA/ comparison graphically, where the mode for gross EFEM to progress swiftly to the development of a anatomy is 3 on the attitude scale compared with a core syllabus. mode of 5 for embryology. It was suggested that students’ attitudes towards embryology are influ- EMBRYOLOGY AND TERATOLOGY FOR SCI- enced predominantly by their pre-university educa- ENCE STUDENTS tion, mainly in biology classes. The assumption was made that at pre-university there is almost no features strongly in many embryological content within the school curricu- biomedical science degree schemes. Indeed, lum; whereas (gross) anatomy is taught at least to some universities nowadays have distinct bachelor some extend in secondary school. Furthermore, degree schemes in the discipline and their appear- gross anatomy is often anchored in the minds of ance signals the major research endeavours being the general population by such different means as undertaken. Clearly, students studying embryology permanent anatomical museums or temporary ex- as part of a science degree require core hibitions, broadcasted documentaries, etc. This is knowledge in excess of that needed for students not the case for embryology. The conclusion was on healthcare schemes. More importantly, since reached that teachers, medical educationalists, many science students would be expected to con- and devisors of medical curricula need to pay spe- sider careers in research (either as researchers or cial attention to informing students of the technicians), practical training in embryological significant role played by embryology in attaining experimental techniques is core and goes beyond clinical competence and achieving the knowledge just knowledge and understanding of embryologi- and understanding of the biomedical sciences that cal facts. A further important consideration is the underpin such clinical areas as obstetrics, paediat- necessity of going beyond core material and to rics and teratology. Consequently, the importance take the students to the frontiers of knowledge. of embryology must be stated explicitly at the start This is best accomplished by allowing their teach- of their course and must be often reinforced, in- ers to expand upon the core syllabus by a more cluding by having embryological topics reintro- detailed, discursive and critical appraisal of their duced at various stages of medical education. Per- own areas of interest and expertise in embryology. haps one way of gaining the attention of the stu- Finally, it is important for a science student to ap- dents towards the importance of embryology and preciate the cultural, historical and philosophical/ teratology is to highlight some of the ethical issues ethical approaches relating to the discipline. that relate to the discipline. In this regard, we would advocate that the students should be en- CONCLUSIONS AND RECOMMENDATIONS couraged to debate ethical issues such as embry- onic tissue sampling and collection, legal limita- The following points relate to the need to teach tions, the use of experimental models, the embryology and teratology and how to teach the use of embryonic stem cells, cloning and genetic subjects: engineering, and eugenics. 1. Medical students require embryology and ter- atology to understand clinical situations that EMBRYOLOGY AND TERATOLOGY FOR DEN- traditionally relate to obstetrics and paediat- TAL STUDENTS rics, but also to appreciate new therapeutic approaches (e.g., intra-uterine therapy; stem Many of the issues that we have raised for the cell therapies). Other healthcare professions medical curriculum also apply to the dental curricu- (such as dentistry) require specialist courses lum, but dental students clearly require much less tailored to their clinical requirements; understanding or knowledge of embryology and 2. Students are better able to understand gross teratology than medical students (except for topics anatomy if they have knowledge of normal that relate to the head and neck). There are how- embryology. Accordingly, gross anatomy and ever specialisations that require greater under- embryology should ideally be taught together; standing and knowledge because of clinical neces- 3. Environmentally, and increasingly in a con- sity. In particular, the dental student should have a sumerist, information-rich, politicised society, good education relating to craniofacial develop- teratology plays a significant role in improving ment. This however requires that some elements the health and well-being of the developing and principles of general embryology are taught to foetus, the new born and the developing child; enable a full understanding of the craniofacial spe- 4. The best methods for teaching embryology cialisations. We advocate therefore that the dental are not simply didactic methods but are prac- student is taught such topics as , so- tical methods that also use animations to aid mites, and the neural crest. Presently, the students’ 3D appreciation of the complexi- a core syllabus for embryology and teratology for

87 Anatomical Education

ties underpinning embryogenesis and organo- versity Press, Oxford, New York; Moore, KL, Persaud TVN, Torchia MG (2015) The Developing Human - Ori- genesis; th 5. Enthusiastic teachers, who are preferably clin- ented Embryology, 10 ed., Elsevier Saunders, Amster- ically qualified, are needed. Furthermore, the dam. 3Fraher J (2007) Anatomy 2020. Anastomosis [ASGBI teachers require motivated students, and evi- newsletter], Spring 2007: 6-7 also Anatomy 2020: The dence suggest that presently the less than view from across the pond. American Association of positive attitudes toward the clinical relevance Anatomists News , Autumn 2007: 1,10. of embryology needs to be addressed before 4This relates to the concept of ‘research-led teaching’ for the students study embryology and teratology; which there is an extensive literature (see Zamorski B 6. It is important that clinicians and embryolo- (2002) Research-led teaching and learning in Higher gists use similar terminologies that are recog- Education: a case. Teach Higher Edu 7: 411-427; Miller nised internationally; A et al . (2012) What is research-led teaching? Crest 7. There is an urgent need to develop flexible, Publications, Kettering, UK; Entwistle N, Ramsden P (2015) Understanding student learning. Routledge, Lon- core syllabuses for embryology and teratology don.) that, having international acceptance, are 5The reader can access many journals specialising in seen to be educationally and politically im- medical and anatomical education (e.g. Medical Educa- portant; tion; Anatomical Sciences Education; Annuals of Anato- my; Clinical Anatomy; European Journal of Anatomy). In The next points reinforce our belief that the sci- addition the reader is referred to Chirculescu ARM, Chir- entific basis of embryology and teratology should culescu M, Morris JF (2007) Anatomical teaching for exist as well as its clinical context: medical students from the perspective of European Un- 1. Following developments throughout the world ion enlargement, Eur. J. Anat . 11: 63-67. Furthermore, a 36 special issue on Anatomical Education was published in (e.g. The Flexner Report in the US ), there is 2014 by the Journal of Anatomy (volume 224 (3)). a strong view that medicine should be a uni- 6http://www.ifaa.net/index.php/fipat; http://www.unifr.ch/ versity-based course. This was proposed to ifaa/; FIPAT is constantly reviewing and developing ter- ensure the delivery of professional, scientifi- minologies, including Terminologica Anatomica (2 nd edi- cally based courses that resulted in medical tion: 2011), Thieme, Stuttgart; Terminologica Histologica practitioners being well-rounded and learned (2008), Lippincott Williams & Wilkins (Wolters Kluwer, Alphen van den Rijn); persons respected as such in society. Bio- 7 medical courses such as embryology and ter- FIPAT’s Terminologica Embryologica (2013) is pub- atology help to deliver this, particularly if the lished by Thieme, Stuttgart. 8See endnote 19 and also Carlson BM (2014) Human student receives research-led teaching; Embryology and Developmental Biology, 5 th Edition, 2. Medicine, as for other healthcare disciplines, Elsevier, Amsterdam. is not just a disease-based discipline, but is 9Drake RL et al. (2002) Survey of gross anatomy, micro- also concerned with functionality and health. scopic anatomy, , and embryology course In terms of embryology, it is important that the in medical school curricula in the United States. Anat student should understand normal develop- Rec, 269: 118-122; Drake RL et al. (2009) Medical edu- ment in advance of being introduced to clini- cation in the anatomical sciences. Anat Sci Educ, 2: 253 cal cases; -259; Drake RL et al. (2014) An update on the status of 3. All students should be exposed to scientifical- anatomical sciences education in United States Medical Schools. Anat Sci Educ, 7: 321-325. ly- and clinically-relevant courses in embryolo- 10 Chirculescu ARM, Morris JF (2008) The curriculum in gy and teratology that take them to the fron- anatomy for medical students: UK and Irish responses tiers of knowledge. This may be delivered in to the ASGBI questionnaire. J Anat , 213: 348; Chir- several ways, e.g. by healthcare courses that culescu ARM (2010) Lecture Notes on General Embryol- have graduate entry, by having 3 years of ogy and Functional Anatomy of the Musculo-Skeletal scientific training before clinical training, or by System. Tehnoplast Publ. House, Bucharest, ISBN 978- 973-8932-48-7, pages 22-25. a programme of students opting out to pursue 11 intercalating science degrees. Spencer J (2003) Learning and teaching in the clinical environment. BMJ , 326: 591. 12 See the recommendations of the General Medical ENDNOTES Council in the UK: GMC (2009) Tomorrow’s Doctors:

1 Outcomes and Standards for Undergraduate Medical As well as the numerous journals concerned with ob- Education. Regulating Doctors, Ensuring good medical stetrics and gynecology in general, there is an academic practice (3 rd edition). General Medical Council, London. journal that deals specifically with this aspect of medi- 13 McHanwell S et al . (2007) A core syllabus in anatomy cine - Journal of Prenatal Medicine published by CIC – adding common sense to need to know. Eur J An- Edizioni Internazionali. In addition, there are journals of at ,11: S3-S18; Smith CF et al. (2015) Anatomical Socie- teratology (e.g. Teratology published By Wiley and Neu- ty core regional anatomy syllabus for undergraduate rotoxicology and Teratology published by Elsevier). 2 medicine: the Delphi process. J Anat , 228: 2-14; Smith References to this view are very numerous, for exam- CF (2016) A new core gross anatomy syllabus for medi- ple: Wolpert, L (1991) The Triumph of the Embryo . Ox- cine. Anat Sci Educ, 9: 209-210. ford University Press, Oxford, New York. Wolpert, L, Tickle C (2011) Principles of development . Oxford Uni-

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14 Leonard RJ et al . (2000) A clinical anatomy curriculum and dental students toward the clinical importance of for the medical student of the 21 st century: developmen- gross anatomy and physiology. Clin Anat, 27: 976-987. tal anatomy. Clin Anat, 13: 17-35; Griffioen et al . (1999) 29 Gasser RF (2010) Digitally Reproduced Embryonic General plan anatomy objectives of the teaching of Morphology (DREM) - A DVD-ROM database of human anatomy/embryology in medical curricula in the Nether- embryo serial sections. Computer imaging laboratory, lands. Eur J Morphol, 37: 228-325; Orsbon CP et a l. and Anatomy, LSU Health Science Center, (2014) Physician opinions about an anatomy core curric- New Orleans, LA, USA, and http// ulum: a case for medical imaging and vertical integra- virtualhumanembryo.lsuhsc.edu tion. Anat Sci Educ, 7: 251-261. 30 This is outlined in Chirculescu ARM (2012) The need 15 Moxham BJ et al . (2014) An approach toward the de- to use stages when teaching embryology. J Anat, 221: velopment of core syllabuses for the anatomical scienc- 315 es. Anat Sci Educ, 7: 302-311. 31 O’Rahilly R, Bossy J, Müller F (1981) Introduction a 16 Tubbs RS et al. (2014) The development of a core l’etude des stades embryonaires chez l’homme. An in- syllabus for the teaching of to troduction to the staging of the human embryo, Bull As- medical students. Clin Anat , 27: 321-330; Tubbs RS, soc Anat , 65: 189; O’Rahilly R, Müller F (1987) Develop- Paulk PB (2015) Essential Anatomy of the Head and mental stages in human embryos, Carnegie Inst. Wash- Neck: The Complete Delphi Panel List. Clin Anat , 28: ington Publ., 637; O’Rahilly R, Müller F (1992) Human 423. Embryology and Teratology, John Wiley & Sons Inc. 17 Moxham BJ et al. (2015) A core syllabus for the teach- Publ.; Gaubert-Cristol R, (1990) Essai d’identification ing of neuroanatomy to medical students. Clin Anat, 28: chez le rat, des stades embryonnaires humains de la 706-716. Carnegie, These de Doctorat en Odontologie, superviser 18 Berman AC (2014) Anatomy of curriculum: Digging to J. Bossy, Universite de Montpellier I. the core. Anat Sci Educ , 7: 326-328. 32 Chirculescu ARM, Chirculescu M (2010) Comparison 19 Carlson BM (2002) Embryology in the medical curricu- between main standard steps of the human pituitary lum. Anat Rec , 269: 89-98. development and hormone specific cells differentiation 20 The Collected Works of John Dewey 1967-1991 , Jo during embryonic period, XXIth Symposium on Morpho- Ann Boydston, ed., Southern Illinois University Press, logical Sciences, Taormina / Messina, Sicily, , Sep- Carbondale. tember 18-22: abstract book printed by Univ. of Messi- 21 Moxham BJ et al . (2011) The future of clinical anato- na, Italy, p. 14; Chirculescu M, Chirculescu ARM (2010) my. Eur J Anat, 15: 5-22. 3D reconstruction evaluation of two key stages in the 22 Moxham BJ et al. (2016) An assessment of the ana- development of the human and rat pituitary during em- tomical knowledge of laypersons and their attitudes to- bryogenesis, Acta Endocrinol. (Buc.) , VI, 2: 14-15. wards the clinical importance of gross anatomy in medi- 33 Agarwal A et al. (2015) Elective courses for medical cine. Ann Anat, 208: 194-203. students during the preclinical curriculum: a systematic review and evaluation. Med Edu Online, 20: 26615 – 23 Flexner A (1910) Medical Education in the United http://dx.doi.org/10.3402/meo.v20.26615 States and Canada: A report to the Carnegie Founda- 34 Moxham BJ, Pias D (2016) How optional should re- tion for the Advancement of Teaching. Bulletin No. 4, gional anatomy be in a medical course? An opinion The Merrymount Press, Boston. piece. Clin Anat , 29: 702-710. 24 Chirculescu ARM, Z ăhoi D, Chirculescu M (1999) The 35 There is an extensive literature developing with re- abnormal ontogeny of the nervous system – malfor- spect to the effects of Zika virus. A recent example is: mations, heterotypes and other abnormalities of the cen- Sarno M (2016) Zika Virus Infection and : A tral and peripheral nervous system. Editura Brumar, Case of , Hydranencephaly and Fetal Timi șoara: 10-18. Demise. PLOS Neglected Tropical Diseases . http:// 25 Chirculescu ARM et al. (2000) The normal ontogenesis dx.doi.org/10.1371/journal.pntd.0004517 of the nervous system - normotype of the central and 36 Drake RL (2014) A retrospective and prospective look peripheral nervous system. Editura Brumar, Timi şoara: at medical education in the United States: trends shap- 17. ing anatomical sciences education. J Anat, 224: 256- 26 Moxham et al. (2016) The attitudes of medical stu- 260. dents in Europe toward the clinical importance of embry- ology. Clin Anat, 29: 144-150. 27 Hattie J. (2009) Visible Learning. Routledge, London. 28 Patel KM, Moxham BJ (2008) The relationship be- tween learning outcomes and methods of teaching anat- omy as perceived by professional anatomists. Clin Anat , 21: 182-189; Moxham BJ, Moxham SA (2007) The rela- tionships between attitudes, course aims and teaching methods for the teaching of gross anatomy in the medi- cal curriculum. Eur J Anat, 11: 19-30; Kerby J et al. (2010) The relationships between learning outcomes and methods of teaching anatomy as perceived by med- ical students. Clin Anat, 24: 489-497; Moxham BJ et al . (2011) The future of clinical anatomy. Eur J Anat, 15: 5- 22; Moxham BJ, Plaisant O (2007) Perception of medi- cal students towards the clinical relevance of anatomy. Clin Anat , 20: 560-564; Olowo-Ofayoku A, Moxham BJ (2014) Comparisons between the attitudes of medical

89 Anatomical Education

Table 3. A Suggested Core Embryology Syllabus for the Dental Course

PRINCIPLES OF EMBRYOLOGY AND PURPOSE OF STUDY IN DENTISTRY

The meaning and importance of embryology and teratology Embryology in the context of human development and growth Outline of the early aspects of implantation and embryonic development Formation of the inner cell mass, and blastocyst The bilaminar disc – epiblast and Formation of the amniotic and yolk cavities GASTRULATION

Purpose of gastrulation The primitive streak, the and the The appearance of the buccopharyngeal and cloacal membranes Migration of epiblast cells at the primitive streak Formation of the germ layers and the trilaminar disc Formation of , , Lateral plate mesoderm development into splanchnopleuric and somatopleuric mesoderm Concept of the role of signalling molecules during gastrulation

DEVELOPMENT OF THE NERVOUS SYSTEM

Role of the notochord Development of the neural plate and hinges Development of the neural tube The neuropores Neural; tube landmarks – prosencephalon, mesencephalon, rhombencephalon The appearance of the Brain flexures Development of the neural crest and the characteristics of neural crest cells General derivatives of the neural crest The role of the neural crest in craniofacial and dental development Early sense organ development – the ectodermal placodes Development of the nasal pit Early Inner development EMBRYONIC FOLDING

Head, tail and lateral folds Appearance of the , and and the outcome of development of the PARAXIAL MESODERM AND THE

Formation from paraxial mesoderm that shows a segmented pattern but not in the developing head region where the paraxial meso- derm remains unsegmented Definition of a and the division into a ventral sclerotome that forms and vertebrae and a dorsal dermomyotome that forms and

90 B. J. Moxham et al.

DEVELOPMENT OF THE PHARYNGEAL ARCHES

Alternative names Appearance on either side of pharyngeal foregut as mesenchymal thickenings Origin of the of the pharyngeal arches and the role of the neural crest 5 pairs and their numbering Ist arch forming maxillary and mandibular processes Derivations of the Derivations of the pharyngeal arch skeletal muscle primordia Derivations of the pharyngeal arch nerves Derivations of the pharyngeal arch aortic arch arteries The pharyngeal pouches and their derivatives The branchial clefts and membranes and their derivatives Branchial cysts Treacher Collins sequences Pierre Robin syndrome CRANIOFACIAL DEVELOPMENT

Formation of the and the fate of the Development of the (including innervation and musculature) and the thyroid gland cysts, ectopic thyroid tissue (incl. lingual thyroid) Formation of the facial processes and the upper Clefts of the Formation of the nasal cavity Formation of the nasolacimal duct The head – formation of the neurocranium and the sensory capsule Fates of the prechordal, hypophyseal and parachordal cartilages The head skeleton – formation of the viscerocranium Development of the from the common oronasal chamber Primary and secondary Mechanisms responsible for palatal shelf elevation Cellular events associated with fusion of the palatal shelves post-elevation Palatal clefts The aetiology of clefts of the lips and palate and teratogenic influences PRINCIPLES OF TERATOLOGY

Common congenital malformations in the craniofacial region and the roles of genetic and environmental factors Folic acid and its beneficial effects EMBRYONIC STEM CELLS

Therapeutic value of stem cells Origins of stem cells Role of ‘embryonic’ stem cells derived from the periodontal and pulpal connectives tissues in a around the

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