Teaching scientific principles in undergraduate medical education – a scoping review on international examples

Background The growth changing roles of physicians are examples for the relevance of teaching scientific principles in undergraduate medical education. The acquisition of scientific skills is comparably weak in undergraduate medical education. This scoping review addresses the following questions: Which examples on teaching scientific principles in undergraduate medical education can be identified in international literature? What is known regarding their educational success and how can they be integrated into undergraduate medical curricula? Methods A systematic scoping review search was conducted in PubMed. Criteria for eligibility were English or German language, publication in a peer-reviewed journal, publication date after 1 st of January 2000 and the publications had to report educational interventions in undergraduate medical education on one of the following basic scientific principles: searching literature, formulating scientific questions, reading and critical appraisal of literature, writing, presentation and understanding of the research process. After full-text screening, 29 studies were included in the analysis.

3 scientific principles in medical education can be fostered by integrating different didactic approaches, by including self-study time and by integrating these principles vertically in undergraduate medical curricula along with clinical aspects.

Background
Today physicians are expected to fulfill different roles. Next to being clinical experts they should be scholars, health advocates, communicators, collaborators, leaders and professionals, as it is documented in the six CANMedS roles (1). In this framework the role of the scholar is described as the ability to "[…] maintain and enhance professional activities through ongoing learning, critically evaluate information and its sources and apply this to practice decisions, facilitate the learning of patients, families, students, residents, other health professionals, the public, and others, as appropriate, contribute to the creation, dissemination, application, and translation of new medical knowledge and practices" (1, p. 645).
In traditional medical education, the facilitation of basic knowledge and its clinical application have played major roles so far, while education in science and scientific principles has not been emphasized (2). Some authors point out that scientific principles are rarely taught in comprehensive ways at medical schools (see for example 3,4). This is changing. Internationally a stronger call for Evidence-based Medicine (EbM) and the constant growth of medical knowledge make it almost indisputable to educate medical students in scientific principles (5)(6)(7)(8). Future doctors need to learn and understand how to handle and to navigate through increasing information and how to assess quality and relevance (4,9). University education in medicine should enable all students to develop basic scientific understanding regardless of later career choices (10). Medical schools are expected to "[…] equip students with knowledge, skills and habits of mind to integrate new scientific discoveries into their practice […]" (11, p. 1).
A recent systematic review by Stone and colleagues on student attitudes towards research in undergraduate medical education shows that students are interested in and generally have positive attitudes towards research (12). On the other hand, many students do not feel well prepared to handle scientific results or interpret findings (3,10,13). At the same time teachers and medical 4 faculties regard competence in generic scientific skills as highly relevant for medical students. These include the ability to systematically collect information on the current state of research, the critical appraisal of scientific publications as well as presentation and critical discussion of results (14). There seems to be a gap in medical education when medical faculty highly value the role of scientific principles in medical education but students do not feel well prepared in scientific skills.
The understanding and knowledge of fundamental scientific principles is a precondition for the successful integration of EbM in medical education and future everyday medical practice (14).
Understanding scientific principles is a universal tool and should be a first step in scientific education (see 4,16). Core ideas of scholarship include experience in literature search, ability to formulate questions, reading and critical appraisal, scientific writing and presentation and a basic understanding of the research process (4,16,17). These core ideas represent basic scientific principles and can be considered as prerequisites in order to fulfill all five steps of EbM (ask clinical questions, aquire evidence, critical appraisal, apply evidence, assess and reflect). To avoid confusion, the term scientific principles in medical education relates to these aforementioned aspects of science. The term basic sciences in medicine is commonly used to address aspects of medical undergraduate education such as basic anatomy or biochemistry and relates to fundamental medical knowledge (18,19).
This scoping review addresses the following questions: Which examples on teaching scientific principles in medical education can be identified in international medical education literature? How can these principles be integrated in undergraduate medical curricula and are educational strategies in teaching basic principles of science successful? By answering these questions, the review is intended to be a helpful tool for readers who are interested in integrating basic principles of science in medical education. There is a need to identify potentially fruitful examples of teaching the scholarly role in medical education and to successfully integrate these into undergraduate medical curricula in order to foster the desired learning outcomes.
There have been reviews on teaching scientific principles in medical education, but regarding the progression and continuing development of medical studies both have to be considered as outdated 5 (17,20).

Methods
A scoping review can be used in order to investigate a body of literature that has not yet been reviewed and which is characterized by a complex and heterogeneous nature (21). "[…]Scoping reviews are an ideal tool to determine the scope or coverage of a body of literature on a given topic and give clear indication of the volume of literature and studies available as well as an overview of its focus" (22, p. 2). It is used to map research findings and literature in a given field. In terms of teaching scientific principles in medical education the scoping review can inform practice (i.e. educators and faculty) about the way teaching has been conducted and organized and what type of evidence can be reported (22). This review is interested in describing concepts of educational interventions on scientific principles in medical education rather than summarizing the evidence and assessing the appropriateness of specific educational interventions. Moreover, terms and definitions in the field of teaching science in medical education are not well established, which is another reason for conducting a scoping review.
Searching for educational interventions on scientific principles in undergraduate medical education cannot be based solely on EbM interventions, as these often include postgraduate training, clinical care and patient-centred approaches that do not necessarily encompass the basic scientific principles named above. On the other hand, science in medicine is a very broad field and it is not clear what kind of evidence can be expected and reported.
The systematic scoping review on current and international examples of teaching basic scientific principles in medical education follows PRISMA guidelines and adheres to AMEE guidelines (6,23).
All publications from January 1st 2000 until May 1st 2019 were included in the search. Earlier reviews on the topic (17,20) were main reasons for time restriction of the search. Search terms were formulated based on the core ideas of scholarship named above. Search terms used were "medical education", "teaching science", "scholar", "scientific principles", "reading", "writing", "critical appraisal", "evidence" and "research" (see appendix 1 for complete search term).
Search was restricted to title and abstract. This search was complemented by MeSH-terms "undergraduate medical education", "medical students" and "research". In this case search can not be restricted to MeSH-terms as these were unspecified for publications regarding the teaching of scientific principles.
In a further step, results of both searches were merged and duplicates removed.  Table 1, an overview and short description of the publications and their educational interventions is presented.   (24) to full-grown vertically integrated study programs (25)(26)(27)(28).
Educational strategies included up to 270 teaching hours across 6 study years dedicated to teaching scientific principles and EbM in medical education (28). Description of the educational interventions varied from very specific to global and broad. Specific descriptions of interventions were found when the program included few teaching hours and was designed for very specific reason, while broader and global descriptions were found for full study programs.
A majority of educational programs was mandatory (N = 16). Three publications presented elective summer schools developed for students with interest in research and scientific projects (16,29,30) Timing of educational interventions was most often between 1st and 3rd study year. In three of the identified curricular interventions teaching of science is spread across more than three study years, as for example in the full study program on EbM described by Marusic (28).
Not all publications included evaluation data. Data regarding outcomes of the educational intervention or indicators of successful implementation of the educational strategy were lacking in 13 studies (see Tables 1 and 2). Evaluation data were included in 16 publications (see Table 2).
Outcomes included measures of student satisfaction, pre-and post-measurement of student knowledge, measures of scientific competence based on tested instruments and randomized trials testing different standards of educational interventions (see for example 31,32). Results were quite heterogeneous: some studies showed improvement in student competencies regarding basic principles of science (see for example 29,30,33,34), some were able to identify higher competencies in intervention groups (but no improvement over time, see for example 24,32,35,36), while others did not find any sort of higher or improved competencies through their educational intervention (see for example 31,37).  What can be learned from this scoping review? When looking at the educational interventions that included substantial evaluation (pre-and postcourse measures or control-group setting) and which showed positive effects regarding outcomes such as students' knowledge or attitude, some common characteristics of these interventions can be identified. Students acceptance of scientific principles in medical education and students practice of scientific skills such as literature search can be fostered by integrating different didactic approaches, such as peer-to-peer teaching, blended learning or virtual patient cases (29,31,40). Accordingly, these diverse didactic formats should be integrated when planning medical curricula, if suitable. For example small group exercises, with students working together in order to understand and critically analyze a scientific paper or publication, support collaboration with only minimal intervention by faculty (see for example 35). Self-study time and the possibility to practice skills such as literature search or critical appraisal are essential for students to develop an understanding of evidence in medicine and to adopt these skills (26,31,37,40,41). Educational interventions should plan sufficient time for self-practice so that students achieve a sense of mastering of relevant tools or databases (24,40). Integrating digital resources and demonstrating their use and relevance for patient care has also been shown to be a promising way, especially when students have the opportunity to integrate their theoretical knowledge into real-life cases (24,31,40). By doing so, scientific principles and research can be linked to practical interventions (24). This includes question formulation based on clinical problems or medical information as well as integrating a literature search and the critical appraisal into patient settings such as bed-side teaching. Educational interventions should not only focus on extending students' knowledge on scientific principles, but also on changing students´ attitudes towards them. Students who adapt an understanding and a positive attitude towards these skills are more likely to integrate them in their future medical practice. As changing attitudes might be a goal that needs a longer period of time, vertical curricular integration of scientific principles in medical education appears most promising.
This is addressed in the hierarchy of evidence based medicine teaching (43). Most evidence supports the notion of interactive learning, with integration of EbM teaching into clinical teaching. Examples of successful interactive integration can be found in this review (33,41). Compared to knowledge, attitudes are harder to assess. A possible form of assessing such soft skills can be student portfolio.
Portfolio enables faculty to document the development of learning objectives such as the ability of critical thinking and attitudes towards EbM which are not easily covered by standard evaluations or written exams (27).
Integration of scientific principles in bedside teaching is possible if web-based information resources are accessible and if teaching staff is well trained (see (33,44,45). Motivation for self-directed learning of students can be triggered by handouts, resources such as critically appraised topics (CAT) or abstracts or short presentations that integrate a clinical case. Structured feedback on the process and results should be given by teachers and instructors.
The development of scientific curricula in existing medical study programs is an ongoing process.
Often, different aspects of scientific principles have been taught within existing educational programs but little effort has been invested in linking these educational parts into a vertically integrated scientific curriculum. Vertical integration of scientific principles allows faculty to lay the basics in early study years and to build up on these aspects in the forthcoming years of the program, allowing students to develop skills step-by-step. This process can be fostered by curricular mapping or curricular inventory (see for example 14). A modular integration of scientific skills enables students to draw connections to clinical care and to experience its clinical relevance, as presented in this review.
By doing so, integration of scientific principles does not necessarily lead to a higher amount of teaching hours per student in an already crowded medical curriculum (33,42,46).
Since an early review of Green on graduate medical education training and evidence-based medicine in 1999, the importance of scientific principles and evidence in medical education has grown. Green

Limitations
Transmission of findings from international publications is difficult as formal and structural aspects of medical studies vary considerably. Medical students in Canada or USA attain a bachelor degree often before entering medical colleges. This is not the case in most European countries. There is also high variation in international medical curricula (47). On the other hand, international consensus is placed on the scholarly role of medical doctors. There are defined characteristics that are of global relevance (1,15). Therefore, a foundation of scientific principles should be based on internationally comparable outcome frameworks (15).
Reporting strategies of the educational interventions differed substantially. Some studies report precisely, describe the educational intervention and present evaluation data including pre-and postmeasures of student knowledge and student attitude (32,34,38,41). Others characterize the intervention briefly and present post-course evaluation data of student satisfaction (35,(48)(49)(50) or report on the educational intervention without any kind of evaluation (25,28,51). A number of tools for assessing student competencies in EbM have been developed such as the Berlin tool and the Fresno test (52-54), but they are rarely applied in the studies included in this review. Only 16 out of 29 22 studies included evaluation data, all other publications did not present any measures at all. This makes a comprehensive analysis of the interventions found a difficult task. Further research is needed, especially regarding questions of educational strategies, integration and successful implementation into existing curricula. It has been noted before that publication of these trials in medical education, especially with a focus on EbM-interventions, lack accuracy in reporting interventions (54). The classification rubric for evidence-based practice assessment tools in education (CREATE) is a framework which provides recommendations regarding assessment of educational interventions in EBP. Different assessment categories are named, amongst them attitudes, knowledge, skills or benefit to patients. Methods of assessment can range from self-report to performance assessment, activity monitoring up to patient-oriented outcomes (7). A variety of instruments to measure students skills in, knowledge of and attitudes towards EbM exist (38). These instruments should be used to reflect the success of educational interventions on scientific principles.
It remains unclear when and how scientific principles should be addressed in medical education (33,55). Introduction in early undergraduate level can be problematic, as it concurs with other basic and medical skills and students might not develop an understanding of its later clinical relevance (55). In postgraduate level introduction can be problematic as it concurs with clinical care.
Nevertheless, the latter has been shown to improve not only skills but also attitudes and behavior regarding EbM (38,54).

Conclusions
This scoping review resulted in a multifaceted and diverse overview on current examples of teaching scientific principles in undergraduate medical education. Based on these results, some practical suggestions on the integration of these principles in existing medical curricula can be named here: Integrate scientific principles vertically in the medical curriculum so that forthcoming teaching can build upon basics (27,33,35).
Plan sufficient amount of time for the teaching of scientific principles (28,56).
Evaluate and use feedback and integrate new forms of evaluation, such as attitudes towards scientific principles in student portfolio (27,31,55).
Give students the opportunity to integrate clinical knowledge and allow for clinical transfer (33,41).

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These suggestions support the successful integration of scientific principles in undergraduate medical

Consent for publication
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Availability of data and materials
All data generated or analysed during this study is included in this published article [and its supplementary information files].