Educational Methods for Teaching Focused Cardiac Ultrasound to Medical Students: A Systematic Review of Efficiency, Scalability, and Outcomes

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Brooks, David Canty, Doa El-Ansary, Alistair Royse, Karen Scholz, and 2 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-7521606/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Background Focused Cardiac Ultrasound (FCU) is increasingly incorporated into medical curricula, yet widespread adoption is limited by faculty availability, teaching resources, and curriculum overload. This review aimed to identify and evaluate current educational strategies for teaching FCU to medical students, with a focus on efficiency, scalability, and diagnostic outcomes. Methods We conducted a systematic review following PRISMA guidelines. Eight databases were searched including PubMed, MEDLINE, Scopus, EMBASE, Web of Science, Cochrane Central, Google Scholar, and clinical trial registries. Eligible studies included those involving undergraduate or postgraduate medical students learning FCU, reporting on teaching methods, learning outcomes, diagnostic accuracy, or resource use. Data were extracted independently by two reviewers. Risk of bias was assessed using the CASP checklist for qualitative studies, STARD for diagnostic accuracy, and CONSORT scoring for randomized controlled trials. Results From 6,700 records, 99 studies were included. Teaching methods included didactic sessions (73%), hands-on practicals (85%), flipped classrooms (39%), simulation (23%), peer mentoring (12%), and self-directed practice (18%). Eleven randomized controlled trials compared different modalities; simulation and online learning were frequently found to be non-inferior to traditional teaching. Simulators and flipped classrooms were associated with increased scalability and reduced faculty time. Peer-assisted learning and curricular integration showed promise, but evidence remains limited. Only 13 studies assessed diagnostic accuracy, with small sample sizes and varied outcome measures. Objective image quality scoring tools were used in 14 studies and may facilitate future standardization. Conclusions Educational strategies such as flipped classrooms, simulation, and peer teaching show potential for scalable FCU education in medical schools. However, methodological heterogeneity and limited high-quality comparative studies restrict firm conclusions. Larger, well-designed trials and diagnostic accuracy studies are needed to determine the most effective and sustainable approaches for widespread FCU integration. Figures Figure 1 Figure 2 Introduction Focused Cardiac Ultrasound (FCU) is emerging as an important bedside tool in medical schools around the world. A recent survey of medical curricular administrators in the United States ( 1 ) found 62.2% of respondents had ultrasound as part of their academic teaching. Whilst studies report the clinical benefit of FCU( 2 – 6 ) there are barriers to implementing FCU skills and competency training in medical programs with large cohorts. Because of a reliance on face to face contact, along with the required training time, FCU has proved to be an expensive and time consuming inclusion in programs( 7 ). Funding requirements for equipment and faculty along with busy medical curricula have impeded the widespread integration of FCU( 1 , 8 ). As such, there is a need to define modes of teaching FCU with a focus on efficiencies and scalable methods of teaching large cohorts of medical students (MS). We conducted a systematic review of the literature to identify what educational modes of delivery are currently in use. Specifically, the primary aim of this review is to describe the teaching methods currently employed for delivering FCU education to medical students. Learning to perform FCU is a complex task requiring acquisition of both theoretical knowledge and practical skills. This has been defined previously into phases of teaching the following components( 9 ): Knowledge base Image acquisition Image interpretation Integration of these skills into clinical practice. It is proposed that these four categories represent a structure for collecting and reporting information on educational methodology. The secondary aim of this review was to provide information on the relative efficacy of the available educational modes employed in learning and teaching FCU. Where information is available on the resources required for these modalities and/or measures of their effectiveness this was collected and presented also. As part of determining efficiency and scalability an estimate of cost should be calculated. Costs include teacher time, student time, resources used (direct and indirect costs) and equipment. Scalability is hypothesised to be critical for success in implementation of FCU training on a mass-scale. Method Eligibility Criteria: We followed a PICOS framework for inclusion as follows: Patients : Medical students enrolled at any stage in either undergraduate or postgraduate training Intervention : The intervention is education in FCU defined as any form teaching relating to the use of ultrasound to assess the heart Outcome: Outcomes of interest include methods of teaching FCU, resources used (direct and indirect costs), and educational outcomes (FCU ability: knowledge base, image acquisition, image interpretation, integration with clinical practice). Comparison: Most studies will be observational and so there is no requirement for a specific comparator to be included. Study design : Articles were required to be peer reviewed original research including audits (course description), observational studies (both prospective and retrospective, comparative and non-comparative) and interventional studies (randomised and non-randomised). Information Sources: The databases searched were WoS, Scopus, googlescholar, Pubmed, MEDLINE, the Cochrane central trials register and EMBASE. Articles identified in the original search had their references reviewed to identify further studies of potential interest. Where review articles were identified in the original search their references were searched for other studies of interest (Although the review articles themselves are not included in the review) to ensure that other studies of interest were not missed. We will also search clinicaltrials.gov and Australian clinicaltrials.gov.au to identify research in progress. Search Strategy: The search terms used for each database are as follows: (“Medical Student*” OR “Undergraduate*” OR “Postgraduate*” OR “University” OR “Medical School*” OR “Medical Education” Medical Curriculum”) AND (“Echocardiography” OR “Echo” OR “FCU” OR “Focused Cardiac Ultrasound” OR “Ultrasound” OR “FOCUS” OR “POCUS” OR “Point of Care Ultrasound” OR “Sonography” OR “Ultrasonography” OR “HCU” OR “Hand Carried Ultrasound” OR “TTE” OR “Transthoracic Echocardiography”) Each database will be searched by both keywords and relevant MESH headings were available. An example is displayed in Figure 1. Study Records: The exact search strategy used for each database is included as appendix 1. Search results and study records were managed through Covidence and EndNote X8. Our process for including studies throughout the stages of Identification, screening, eligibility and inclusion followed the PRISMA flow diagram included in the results. Once duplicates were removed articles were screened by review of their title and abstract to see if they meet the basic eligibility criteria outlined above. This process was performed by one researcher applying the PICOS framework. Following this articles that passed the screening phase were reviewed for eligibility. This process involved two researchers performing the following process: For papers using a qualitative framework the CASP checklist (Appendix 2.) was be applied. To be eligible to be included both researchers will need to answer YES to questions 1 and 2 in section A. Studies that provided information on diagnostic accuracy of medical students or compare efficacy of different teaching methods in an RCT format were be included by default. For these studies the CONSORT checklist (Appendix 3.) was utilised and each paper given a score out of 30 to grade its methodological quality. Data collection was performed using a standardized tool (appendix 4). This was completed independently by two researchers and the results collated by the primary investigator. Definitions of all criteria and endpoints were agreed by the researchers before performing the search. Outcomes: For this review the primary endpoint of data extraction is the educational techniques used. Secondary endpoints including learning outcomes are described and compared where possible, for example diagnostic accuracy and trials directly comparing different teaching methods are analysed separately. Results The original search produced 6700 articles in total from all databases searched. The flow of these articles through the study is outlined in the PRISMA flow diagram below (Fig. 1). Program Characteristics Demographics of the studies are outlined in table 1 and study characteristics are outlined in table 2. The majority of studies over the last decade have been conducted in the United States. Notably no studies have assessed the feasibility of conducting a dedicated FCU program in Australia. Our review reveals that FCU is currently being taught through all years of medical school in both undergraduate and postgraduate programs. There appears to be an increase in publications over the last decade also with the majority of studies being published since 2015. Further data was collected on randomised controlled trials (RCTs) that compared educational modalities and diagnostic accuracy studies and these are outlined in tables 3 and 4. Despite calls from many authors to improve efficiency and scalability of studies the predominant teaching methods are still didactic lectures and small group teaching of practical skills. To answer our research question, we reviewed alternative methods of delivering teaching for their efficiency and scalability. Very few papers provided information on the costs of the programs and so this analysis was abandoned. Flipped Classroom All phases of learning FCU including image acquisition, image interpretation and integration of findings into clinical practice require the assimilation of theoretical knowledge by the learner. The practice of FCU requires an understanding of the physics involved in sound transmission, the electronics and software utilised in image formation along with knowledge of the anatomy, physiology and pathophysiology of the heart. Thus before learning this practical skill there is a requirement for significant knowledge transfer to the novice practitioner(10). The flipped classroom model of providing online content to learners prior to them attending for practical teaching now appears to be widely utilised to decrease face to face time with 39.2% of studies describing this method. Small Group teaching Teaching image acquisition in FCU is time-consuming and labor-intensive and previously described methods necessitate teaching in small groups(11) with a requirement for many hours of teacher time. Currently the expanding need for skilled educators occurs in conjunction with increasing clinical school class sizes which poses additional challenges. Hands-on courses in image acquisition are demanding on faculty, most of whom are involved in busy practices and other research activities. Integration of this new modality then poses a difficult problem for medical schools that already provide full schedules to students. Currently the most common type of teacher for delivering this content remains doctors who are without doubt the most expensive tutor available despite alternatives existing. Other studies have utilised sonographer and peer mentoring as quantified in table 2. Alternatives to practicing on patients As sourcing sufficient patients or models is often difficult, simulators have been identified as an effective method of teaching larger cohorts. Simulators lend themselves to independent practice by Novice FCU practitioners because they are readily available, avoid consent issues and provide a standardised learning experience. Peer scanning then has also been identified as method of providing high fidelity simulated patients for practice. Integration with existing programs Another approach to produce efficiencies in FCU education is by integrating the teaching of FCU with other existing programs including anatomy, physiology and clinical skills. Many authors have proposed that the already busy curriculums of medical school pose a significant barrier to the introduction of new course material. If FCU could be introduced without detriment to or perhaps even to the benefit of other programs, then this would represent an efficiency in itself. Research Methodology As described in table 2 the majority of research in this field is observational or qualitative. Whilst these studies are still useful in identifying potentially efficient methods they do not offer concrete data on which methods are the most effective or efficient. Only 11 studies compared teaching methods in the context of a randomised controlled trial and only 13 produced information that could be used to assess the diagnostic accuracy of the learners at the end of the teaching program. The most common methods for assessing MS after receiving FCU teaching were written tests or performance on objective standardised clinical exams (OSCEs) and this was uniformly the case in the RCTs identified. For diagnostic accuracy studies student FCU results were usually compared to formal TTE or Cardiologist obtained FCU images. Some studies had experts review the images obtained by the students as a comparator. Discussion Program characteristics Year of medical School Two studies directly assessed whether the timing of FCU training affected Learning outcomes( 12 , 13 ) Byrne’s study of 2019 assessed whether year of medical school affected learners’ ability to learn FCU by dividing them into early and late clinical years of medical school. In Switzerland this relates to years 3 and 4 for vs 5 and 6 of medical school. This study demonstrated that students who were more advanced in their training performed better than students in their early years on written assessments. No difference was found however, when assessing the clinical skill of performing FCU. The difference in written skill may be confounded by other knowledge gained during medical school and the authors concluded that learning the practical skill of FCU can be incorporated at whatever level is most convenient to training( 12 , 13 ). Cawthorn 2014( 14 ) assessed the ability of first and third year medical students to perform FCU and retain knowledge regarding it. They demonstrated that both groups could be taught FCU knowledge and skills. Whilst not directly compared the third-year students in this study showed greater improvement in both knowledge and skills and again the authors attributed this to greater background knowledge gained during other aspects of medical school. In summary FCU is currently being taught in all phases of medical school with no clear evidence of benefit for a particular time point but an indication that students in later years might benefit from the additional experience they have gained in other studies. It may be that the best strategy is to begin early to assist in incorporating more teaching over several years without affecting other curricula adversely. Several studies have described longitudinal programs and these will be discussed separately. Online content In an effort to decrease face to face time for both students and teachers many programs have converted all or a component of their didactic teaching to online content. This may take the form of written content, recorded video lectures, online image libraries or even practical instructional videos. Details of the online content described in the studies vary from brief outlines to detailed descriptions of structured programs. For example the system developed by Beaton( 15 ) utilised on-line image libraries, instructional modules and feedback via interactive quizzes to cover both knowledge transfer and image interpretation ( 16 ). Proponents of online systems emphasise the benefits of asynchronous learning completed at the learner’s convenience thereby enhancing integration with existing busy medical courses. Novel approaches to delivering online content include the use of social media( 17 , 18 ). Bahner 2012 demonstrated that the push technology of Facebook and twitter could be used to deliver online content to learners on a daily basis which received good feedback on qualitative surveys. Hempel conducted a randomized controlled trial evaluating the effectiveness of a "sandwich e-learning" model for point-of-care ultrasound (POCUS) training among 62 medical students. This model combined pre-course e-learning, a one-day hands-on course, and post-course social media–based learning via Facebook. Four groups were compared, varying in access to pre- and/or post-course e-learning. After six weeks, knowledge retention was similar across all groups, but students with post-course social media access reported greater satisfaction. The study supports the feasibility and acceptability of integrating social media into blended ultrasound education, without compromising knowledge retention. There are several studies directly comparing face to face teaching with online programs. Cawthorn’s study of 2013 compared face to face didactic teaching with electronic modules and showed digital content was equivalent to didactic teaching in knowledge transfer for 3rd year medical students. This finding was replicated by Florescu 2014 ( 19 ) who found a video podcast produced equivalent learning outcomes to a face-to-face lecture. Hempel 2014( 20 ) found that online teaching was superior to face to face teaching for knowledge acquisition and no different for practical skills acquisition. Given the perennial nature of online resources and the benefits from asynchronous learning form the flipped classroom model, online learning is likely to be a significant feature of future FCU teaching programs. To date most models of teaching involve face to face contact at some point usually during hands on small group teaching. Indeed, the study by Cawthorn et al( 13 ) that attempted a fully self-directed course found that outcomes were not as good as with some face-to-face teaching. Future research here may need to focus on defining what the minimum instructor time that is required and when this time is best utilised. Small group hands on teaching In the traditional cardiology format of performing TTE a highly trained sonographer acquires the images which are then interpreted by a cardiologist. This system recognises the independent expert skill sets of image acquisition and image interpretation held by the two craft groups. In the educational setting then it makes sense to utilise the specific expertise of both groups also. Whilst many programs have demonstrated the efficacy of using sonographers to provide teaching there have been no trials comparing sonographers to other expert staff to teach image acquisition. Given Sonographers represent a significant cost saving in the delivery of image acquisition training their integration into curriculum warrants further assessment in comparative trials. Most trials utilise ratios of between 1 to 3 and 1 to 5 to deliver practical hands-on training. This Teaching has been delivered by various groups of doctors including emergency physicians, Intensivists, cardiologist and anaesthetists as well as by trained sonographers without comparative trials that might determine a clear benefit of any particular group. Two authors have demonstrated the effectiveness of using digital solutions to increase teaching ratios and thereby produce efficiencies. Utilising a large screen and multiple small screens at each station of students a trial by ( 21 ) Evans demonstrated the effectiveness of a 1:80 ratio of instructors to students. However qualitative feedback from students revealed they wanted closer instruction. Peer Mentoring Identifying sufficient numbers of experienced instructors to teach large cohorts is difficult and represents a barrier to scalability over and above cost. To overcome this several authors have utilised previously trained medical students to assist in delivering teaching to subsequent cohorts( 22 – 24 ). This concept of peer mentoring is not new to medical school and has been adopted widely in the delivery of other curriculae( 25 ). Peer mentors can be identified within a cohort of students receiving a standard teaching program or alternatively some authors have taken the approach of providing specific training in teaching FCU to smaller groups of medical students who then go on to teach a larger cohort. These students have either been identified as being particularly skilled or self-selected from the cohort. Peer mentors have been utilised for both didactic knowledge delivery and for teaching practical skills. However, as image acquisition requires the most face-to-face time it is the component with the most efficiency gains when utilising peer mentoring. The effectiveness of peer mentoring has been assessed in trials comparing it to teaching by experts with mixed results. In a trial comparing teaching by experts to teaching by trained MS it was ( 26 )demonstrated that MS taught by peers showed significantly better FCU skills than expert trained peers. The authors hypothesised that the student teachers found it easier to relate to the difficulties their students encountered and more closely remembered their strategies for overcoming them. Likewise Ahn ( 23 ) found that senior peer instructors received equivalent scores to instructors from students who received their teaching. Conversely the trial by Kuhl et al of 2012 demonstrated that whilst peer teachers could provide teaching that objectively improved MS skill in FCU, this teaching was inferior to that provided by experts. From a qualitative perspective Gradl-Dietsch 2018( 27 ) demonstrated that whilst peer teaching could deliver equivalent educational outcomes on objective measures when asked in qualitative surveys, students would have preferred expert mentors to peer teaching. This is contrasted to the findings of Dickerson ( 28 ) and Fu ( 29 ) who found overwhelming support for peer teaching from MS who received this teaching. The heterogeneity in outcomes using peer scanning may relate to the training and selection of peer tutors. Whilst this method holds promise for improving scalability the best method of achieving this remains elusive. Peer Scanning Several studies have described using peers as live models for scanning. ( 21 , 28 , 30 ). The use of human models for teaching has a requirement for payment and poses a significant burden of logistics in organising models. Medical students however have demonstrated a keenness to participate as models for their peers without payment to facilitate their learning and skill acquisition. Young male medical students usually have good acoustic windows and represent ideal models for demonstrating normal anatomy with FCU. Volunteering as a model may also represent an additional exposure to teaching during the teaching program representing an auxiliary benefit to the MS model( 29 ). Simulators Several studies have now compared simulators to traditional human models for delivering FCU education. Bentley 2015 and Hempel 2020 ( 20 , 31 ) compared simulators to traditional teaching with human models in non-inferiority designs. In these studies there was equivalent transfer of both theoretical knowledge and practical skill. Damewood( 32 ) also demonstrated that the use of a Simulator in FCU education could provide equivalent results to teaching with live models. Their group further proposed that a simulator allows more pathologies to be seen quickly though it can be argued that this can be overcome quickly with an image library. Kusenose ( 33 ) Compared simulator use to textbook learning for didactic teaching and found students receiving the simulator teaching hasd faster scan completion times, improved image acquisition skill and higher satisfaction. The technology embedded in some simulators also provides for novel educational opportunities and simulation has been found to hold unique potential for providing feedback in two recent reviews. ( 34 , 35 )Ellison( 36 ) demonstrated the use of a simulator to give immediate feedback to students after image acquisition to help guide the students probe position. They argued this gives students individualised feedback specific to their need even if they are working without supervision. Whilst this study demonstrated a well-designed educational program that could be approached by students in an entirely self-directed manner unfortunately it did not test students’ ability to obtain images on human subjects as an outcome. The authors propose that their basic training might precede face to face teaching with experts who could then teach more advanced skills or focus on learners who took longer to develop a basic FCU skill set. Cecilio fernandes 2020 also demonstrated that in built feedback technologies could be used for image acquisition teaching to MS. However, in this small randomised controlled trial feedback from experts proved superior to feedback from the simulator. This may be due to expert feedback adding clinical relevance and feedback in context. Le ( 37 ) demonstrated further that Simulators assist knowledge retention when used after a formal ultrasound course. They proposed that the use of simulators as an adjunct to supervised training on live models represented an efficient option for ultrasound training. Providing open access to an ultrasound simulator might permit students to maintain their skills without further supervised training. Jensen ( 38 ) examined the effectiveness of simulation-based training using a mastery learning approach. In this prospective study, 25 medical students with no prior ultrasound experience trained on a virtual-reality simulator until they reached a predefined expert-level performance. Twenty-three participants (92%) achieved mastery within a median of 1 hour and 46 minutes. Despite attaining the competency threshold, examination efficiency (speed) continued to improve with additional training. The findings challenge volume-based training models and support individualized, competency-based ultrasound education. Deiden ( 10 ) used a qualitative framework to explore student’s perceptions and experience with simulator based FCU education. Through focus group interview with medical students they explored themes that defined the main challenges of learning FCU with a view to improving future programs. Student responses highlighted that “play” was helpful to their learning of FCU. The student perception was that without oversight they could freely make, and then learn from, their mistake without prejudice. This concept of allowing students to engage with the simulator in a self-directed manner may be a useful component of future simulator courses. The idea of integrating deliberate discussion of errors as adjuncts to self-directed simulator teaching may also improve knowledge acquisition as it utilises a logical approach to dissecting errors. In summary whilst the best methods of utilising simulators in efficient FCU teaching programs has not been defined there is clear potential for scalable solutions utilising them. Self- Directed Practice Allowing students time to practice independently either with a simulator or US and a human model or patient may be an efficient method of increasing student experience with ultrasound as it promotes self-paced learning and provides the opportunity to learn through repletion and practice. Studies ( 36 , 39 , 40 ) have described this usually incorporating self-directed practice at some point in a program with other supervision or feedback. This process Can be assisted with written handouts describing lessons plans or specific educational goals for self-directed sessions. Future research may shed light on the balance between supervised and self-directed practice as it may be that self-directed practice is more beneficial when preceded by direct supervision. Also the best mechanisms of giving students guidance and feedback during self-directed practice are not yet defined. Remote Teaching Russell( 41 ) conducted a pilot randomized study to assess the feasibility of teaching cardiac ultrasound remotely using Google Glass telementoring. The study demonstrated that telementoring via wearable technology is a viable alternative to in-person instruction for novice ultrasound users. Competition Several studies have described the ( 42 ) ( 43 – 46 )gamification of ultrasound teaching or the introduction of competition to motivate asynchronous self-study of ultrasound (US), qualitative evidence from these studies suggests this may be a cost effective way to improve engagement. Integration with existing medical school teaching. For the following sections only studies that involved the hands-on teaching of FCU were included. Specifically, studies that described teachers utilising ultrasound to demonstrate concepts without teaching students themselves to acquire images were excluded. Teaching anatomy To those who teach FCU the auxiliary benefits of increasing students’ knowledge of anatomy are obvious and several recent studies have demonstrated this. Hammoudi ( 47 ) demonstrated integration of ultrasound to a cohort of 330 medical students using existing faculty resources and the addition of ultrasound machines. The course received excellent qualitative feedback a feature consistent in other studies using qualitative assessment. In the quantitative arena Canty( 48 ) demonstrated that an ultrasound simulator could be used to teach cardiac anatomy with effectiveness equivalent to traditional cadaveric based teaching. The efficacy of ultrasound based anatomy teaching was further demonstrated by Kondrashov( 49 ) with improved scores on an anatomy exam with a before and after study design. Integration with existing clinical skills teaching Most clinical exposure is in ED and ICU( 50 – 52 ) and programs can be set up with minimal additional resource by integrating with existing clinical services in these areas which ordinarily have access to point of care ultrasound devices in a contemporary clinical context. Fu( 29 ) performed qualitative assessments on learners experience in which ED and ICU were identified as exceptional clinical environments for learning FCU. The authors discuss the idea that this clinical context allows the beginning of integration into clinical practice. Notably in our review very few studies discuss how they teach the final step of integrating US findings into clinical practice. Other clinical settings that have been investigated include final year anaesthesia selective( 53 ) and a radiology elective.( 54 ) Improving Clinical Skills When integrated with traditional clinical skills FCU teaching has been reported to improve bedside acumen. Dinh( 55 ) and Liu( 56 ) demonstrated that implementing FCU into a clinical skills curriculum for MS was feasible and could improve student usual beside skills as measured on OSCE’s that formed part of academic assessment. Longitudinal programs Several longitudinal programs already exist( 1 , 57 – 59 ) that range for one year or longer in which FCU skills are integrated with existing programs including anatomy, physiology and clinical skills. These programs build FCU skills on foundational anatomy and ultrasound knowledge gained in earlier years without interrupting existing teaching. Rapaport 2019 identified that FCU image acquisition skills deteriorate over time when not used. As such these integrated programs may well benefit from the continuous exposure of learners to ultrasound over subsequent years. Methodological Considerations Many studies have incorporated a bespoke FCU based OSCE to assess the effectiveness of their teaching intervention. For instance all of the RCTs identified used their own MCQ or OSCE preventing further comparison between trials. These OSCEs are usually a qualitative assessment of images and the process of their acquisition which has the advantage of being rapid but often has a subjective component. Whilst these can assess the transfer of theoretical knowledge and basic procedural skill they do not assess the student’s ability to perform FCU in the real world. Some studies have developed detailed image quality analysis tools as part of an OSCE process solely for the purpose of their study. When such systems already exist this duplication of effort may impede the progress of future research. A more objective measure is the use of a validated image quality score as described in 14 studies in this review. The use of an objective image scoring system allows specific analysis of a student’s skills in image acquisition. This then allows assessment of the effectiveness of different educational modalities particularly when the scoring system allows quantitative assessment over a broad range of image quality. Image quality scoring Systems that only use categorical analysis of image quality do not allow finer analysis of image quality particularly at the higher end of quality. Ie systems that simply grade whether depth and gain have been adjusted adequately or whether a particular structure can be identified and labelled do not have the same discrimination as systems that analyse whether all the anatomical structures usually identified in a particular echo view can be identified. Where simulators are employed it is possible to assess a learner’s image by analysing their probe position and angle relative to an ideal view. Hence other authors have sought to uses in built technology in simulators to assess students( 36 , 60 ). This has the advantage of rapid computer assisted analysis of image quality but the disadvantage of not measuring real world conditions that exist due to the variability in human anatomy between patients and even models. Whilst image libraries can be used for image interpretation this does not account for the cognitive load associated with performing and interpreting the scan simultaneously. The effects of cognitive load are likely to be more marked with novice learners. Diagnostic Accuracy Diagnostic accuracy studies tended to have a smaller number of students with an average class size for diagnostic accuracy studies of 16.4 compared with the average a class size of 89.2 for other studies. This presumably relates to the increased burden of performing a formal diagnostic accuracy study but reveals that accuracy of large cohorts of students learning FCU has not been assessed. Panoulas 2013 – showed that brief intervention improved bedside assessment over and above history and examination. The aim of this study was to examine whether students could improve their diagnostic accuracy at the bedside with the assistance of FCU. This is consistent with a pilot study by Parks 2015 suggesting that medical learners new to FCU, the addition of the “ACES PoCUS” protocol to standard clinical assessment improved diagnostic accuracy. This is a fundamental question of the benchmark of FCU in this setting. Is the aim of teaching FCU to improve bedside skills with or without the use of ultrasound or should FCU be compared to TTE or simply to existing bedside clinical skills? The latter is poorly defined in terms of diagnostic accuracy and has significant heterogeneity in quality between institutions. The former is a standardised diagnostic test with known accuracy which assists in comparative studies but exists separate to usual bedside skills. Knowing the true diagnostic accuracy of FCU would be enormously useful in deciding where it fits into a diagnostic algorithms and further teaching of bedside skills. As this has not been done formally for traditional bedside skills a Bayesian analysis of diagnostic certainty utilising pre and post test probabilities would be a new endeavour for FCU researchers. These studies may set the bench mark for efficacy of teaching with future studies trying to replicate findings with less resources or greater numbers of students. Costs Few studies give detailed information on the cost of their program. It is often unclear whether resources are shared, existing or bought as new for the project. It is common for researchers to be delivering the educational material in a voluntary capacity often for the secondary gain of generating the research. This is an excellent motivator whilst generating research outcomes it belies the fact the ongoing provision of teaching will have associated costs( 61 ) For instance a feasibility study by Gogalnicaeu ( 61 ) quoted their cost as minimal as the 5 US machines utilised were donated by industry for the project and all faculty participated pro bono. Notably they benchmark costs of a 1 day commercial course in the UK between £250 and £400 per student. These courses are available to undergraduates. Future Research Image quality scoring systems that are previously validated hold the potential to set benchmarks for teaching image acquisition in FCU and ongoing comparison between studies. Although assessing image acquisition and interpretation independently has advantages for analysing the different components of a teaching program unless they are analysed concurrently the results may not reflect student’s future performance in real world conditions. Hence studies targeting diagnostic accuracy with larger cohorts are warranted. Here measures of agreement should be considered. Whilst sensitivity and specificity are immediately recognisable to most clinicians, they may not be the best measures of agreement for these studies. The kappa statistic has been used with good effect to convey chance corrected agreement that takes into account both the prevalence of the pathology and also the size of the sample. There remains a deficit of randomised controlled trials particularly with larger cohorts to define the best methods to teach the large cohorts that exist in most medical schools. Finally, more high quality diagnostic accuracy studies are needed to determine the true accuracy of medical students after receiving this teaching. Conclusion Our review reveals that research in MS FCU teaching is being led by the US and appears to be increasing in volume. Further this research has not yet commenced in Australia. Current evidence suggests that teaching can occur effectively in any year of medical school. This systematic review has identified a number of educational modalities that have the potential to contribute to increasingly efficient educational programs in FCU. For instance the flipped classroom model now appears to be defined as the most efficient method of knowledge transfer and image interpretation. However, the methodological limitations of the majority of studies means that further research will be required to define the most efficient methods of teaching image acquisition and integration into clinical practice. Currently comparison of educational modalities is hampered by the outcome measures used to assess most programs. Written tests whilst useful in assessing theoretical knowledge do not assess a student’s skill level in performing FCU. In this regard objective image quality scoring tools appear to hold the most promise. Widespread use of these tools would allow the comparison between different studies and of educational programs as they are adapted over time. There is a paucity of high quality evidence targeting diagnostic accuracy achieved with FCU by MS. Diagnostic accuracy studies to date have been small and lack generalisability. The use of formal TTE and the kappa statistic to assess for agreements seems to hold promise in the future but trials will need to include larger numbers of students to determine generalisability. Further investigation is warranted to evaluate the feasibility and effects of specific educational modalities for teaching image acquisition, the use of simulators, self-directed practice, engaging peers in scanning and sonographers as educators. The flipped classroom has now proven to be highly acceptable to students and overcomes many of the barriers related to crowded curricula and student timetables. As a perennial resource is may also decrease the annual requirement for face-to-face teacher time. Simulators may provide efficiencies by decreasing the burden on patients or the cost of models whilst maximising the time students can spend practicing and minimising time spent consenting patients. Peer scanning could be the ultimate high-fidelity simulator and has again been shown to be quite acceptable to students. As programs minimise teacher face-to-face time the ideal amount of clinician interaction with the students remains to be determined as does which clinicians should be involved. As sonographers are the experts in image acquisition in cardiology they may represent a potentially cost effective solution. In terms of scalability the use of echo simulator appears to hold the greatest potential for teaching image acquisition. The early success of trials that utilise either in built feedback mechanisms in the simulators or additional teaching materials that facilitate self-directed learning certainly holds promise for defining further scalable and efficient solutions here. It is possible that integration of ultrasound into existing curricula may be an efficient way of teaching. From the perspective of FCU teaching it is likely that learners benefit from the consolidation of skills over time. There also remains a deficit in the research of how FCU skills are integrated into clinical practice. It may be that until diagnostic accuracy is defined in this group there remains a reluctance to incorporate FCU findings into clinical assessment. Conversely where FCU skill is defined, MS may find themselves leading team interaction within assigned teams during ward rounds and other clinical duties. In conclusion further high-quality research is required to define the feasibility and the most efficient methods of teaching FCU to MS. A multi-modal teaching approach involving the flipped classroom, simulators, peer scanning, sonographers as teachers and finally integrated clinical placements to consolidate skills may promote integration and translation of FCU skills into clinical practice. Declarations Human ethics and Consent to participate Not applicable As a systematic review article no participants were directly recruited for this research. Funding No funding was obtained to complete this research Clinical trial number Not applicable. References Bahner DP, Goldman E, Way D, Royall NA, Liu YT. The state of ultrasound education in U.S. medical schools: results of a national survey. Acad Med. 2014;89(12):1681-6. Decara JM, Kirkpatrick JN, Spencer KT, Ward RP, Kasza K, Furlong K, et al. 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Tables Tables 1 to 4 are available in the Supplementary Files section</p Additional Declarations No competing interests reported. Supplementary Files Table1BMCSR.docx Table2BMCSR.docx Table3BMCSR.docx Table4BMCSR.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-7521606","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":528293567,"identity":"c5e4e22a-fa45-45dc-8cac-699205912648","order_by":0,"name":"Kyle S. 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16:12:29","extension":"html","order_by":19,"title":"","display":"","copyAsset":false,"role":"acdc-reference","size":227472,"visible":true,"origin":"","legend":"","description":"","filename":"earlyproof.html","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/f2237b68130e91de477ff79e.html"},{"id":93612549,"identity":"0c9547a9-26d5-4ded-aab0-e7311c30dd25","added_by":"auto","created_at":"2025-10-15 16:20:28","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":105754,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eSearch strategy with MESH headings and key terms.\u003c/strong\u003e\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/11fb264fd12c48d04f3727c5.png"},{"id":93611138,"identity":"8561615b-1efe-4f57-988f-21dc787f6461","added_by":"auto","created_at":"2025-10-15 16:12:28","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":80911,"visible":true,"origin":"","legend":"\u003cp\u003eFigure 1. Prisma diagram of flow of articles through study\u003c/p\u003e","description":"","filename":"01.png","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/3d5deb6c8c8ae60ed4ac708b.png"},{"id":107520213,"identity":"44713f40-6004-4e01-b67c-92dc74873f73","added_by":"auto","created_at":"2026-04-22 08:59:24","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":599808,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/39351133-61dc-47e8-a014-2a2d519b4bec.pdf"},{"id":93611141,"identity":"f7f0f266-81d5-48bd-9045-6106f80edf25","added_by":"auto","created_at":"2025-10-15 16:12:28","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":15163,"visible":true,"origin":"","legend":"","description":"","filename":"Table1BMCSR.docx","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/7e8b45969b9c09615133b063.docx"},{"id":93611142,"identity":"8ab9bb8e-64d6-4156-a2fc-815f7d3dc13a","added_by":"auto","created_at":"2025-10-15 16:12:28","extension":"docx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":16941,"visible":true,"origin":"","legend":"","description":"","filename":"Table2BMCSR.docx","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/d64bc5f37941a12d9ee2c6d5.docx"},{"id":93612554,"identity":"bb588432-5947-4dab-8571-39bb2aa45f87","added_by":"auto","created_at":"2025-10-15 16:20:28","extension":"docx","order_by":3,"title":"","display":"","copyAsset":false,"role":"supplement","size":18194,"visible":true,"origin":"","legend":"","description":"","filename":"Table3BMCSR.docx","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/534d02588bf5126a00b83342.docx"},{"id":93611156,"identity":"bbd3af27-f602-450b-809a-ebba1a2a8439","added_by":"auto","created_at":"2025-10-15 16:12:28","extension":"docx","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":177323,"visible":true,"origin":"","legend":"","description":"","filename":"Table4BMCSR.docx","url":"https://assets-eu.researchsquare.com/files/rs-7521606/v1/9b2eeace83bc5c5fb22961b8.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Educational Methods for Teaching Focused Cardiac Ultrasound to Medical Students: A Systematic Review of Efficiency, Scalability, and Outcomes","fulltext":[{"header":"Introduction","content":"\u003cp\u003eFocused Cardiac Ultrasound (FCU) is emerging as an important bedside tool in medical schools around the world. A recent survey of medical curricular administrators in the United States (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e) found 62.2% of respondents had ultrasound as part of their academic teaching. Whilst studies report the clinical benefit of FCU(\u003cspan additionalcitationids=\"CR3 CR4 CR5\" citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e) there are barriers to implementing FCU skills and competency training in medical programs with large cohorts. Because of a reliance on face to face contact, along with the required training time, FCU has proved to be an expensive and time consuming inclusion in programs(\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e). Funding requirements for equipment and faculty along with busy medical curricula have impeded the widespread integration of FCU(\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e). As such, there is a need to define modes of teaching FCU with a focus on efficiencies and scalable methods of teaching large cohorts of medical students (MS).\u003c/p\u003e\u003cp\u003e We conducted a systematic review of the literature to identify what educational modes of delivery are currently in use. Specifically, the primary aim of this review is to describe the teaching methods currently employed for delivering FCU education to medical students. Learning to perform FCU is a complex task requiring acquisition of both theoretical knowledge and practical skills. This has been defined previously into phases of teaching the following components(\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e):\u003c/p\u003e\u003cp\u003e\u003col\u003e\u003cspan\u003e\u003cli\u003e\u003cp\u003eKnowledge base\u003c/p\u003e\u003c/li\u003e\u003c/span\u003e\u003cspan\u003e\u003cli\u003e\u003cp\u003eImage acquisition\u003c/p\u003e\u003c/li\u003e\u003c/span\u003e\u003cspan\u003e\u003cli\u003e\u003cp\u003eImage interpretation\u003c/p\u003e\u003c/li\u003e\u003c/span\u003e\u003cspan\u003e\u003cli\u003e\u003cp\u003eIntegration of these skills into clinical practice.\u003c/p\u003e\u003c/li\u003e\u003c/span\u003e\u003c/ol\u003e\u003c/p\u003e\u003cp\u003eIt is proposed that these four categories represent a structure for collecting and reporting information on educational methodology.\u003c/p\u003e\u003cp\u003eThe secondary aim of this review was to provide information on the relative efficacy of the available educational modes employed in learning and teaching FCU. Where information is available on the resources required for these modalities and/or measures of their effectiveness this was collected and presented also. As part of determining efficiency and scalability an estimate of cost should be calculated. Costs include teacher time, student time, resources used (direct and indirect costs) and equipment.\u003c/p\u003e\u003cp\u003eScalability is hypothesised to be critical for success in implementation of FCU training on a mass-scale.\u003c/p\u003e"},{"header":"Method","content":"\u003cp\u003e\u003cstrong\u003eEligibility Criteria:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe followed a PICOS framework for inclusion as follows:\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003ePatients\u003c/strong\u003e: Medical students enrolled at any stage in either undergraduate or postgraduate training\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eIntervention\u003c/strong\u003e: The intervention is education in FCU defined as any form teaching relating to the use of ultrasound to assess the heart\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eOutcome: \u003c/strong\u003eOutcomes of interest include methods of teaching FCU, resources used (direct and indirect costs), and educational outcomes (FCU ability: knowledge base, image acquisition, image interpretation, integration with clinical practice).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eComparison: \u003c/strong\u003eMost studies will be observational and so there is no requirement for a specific comparator to be included.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eStudy design\u003c/strong\u003e: Articles were required to be peer reviewed original research including audits (course description), observational studies (both prospective and retrospective, comparative and non-comparative) and interventional studies (randomised and non-randomised).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eInformation Sources:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe databases searched were WoS, Scopus, googlescholar, Pubmed, MEDLINE, the Cochrane central trials register and EMBASE. Articles identified in the original search had their references reviewed to identify further studies of potential interest. Where review articles were identified in the original search their references were searched for other studies of interest (Although the review articles themselves are not included in the review) to ensure that other studies of interest were not missed. \u003c/p\u003e\n\u003cp\u003eWe will also search clinicaltrials.gov and Australian clinicaltrials.gov.au to identify research in progress. \u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eSearch Strategy:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe search terms used for each database are as follows:\u003c/p\u003e\n\u003cp\u003e(\u0026ldquo;Medical Student*\u0026rdquo; OR \u0026ldquo;Undergraduate*\u0026rdquo; OR \u0026ldquo;Postgraduate*\u0026rdquo; OR \u0026ldquo;University\u0026rdquo; OR \u0026ldquo;Medical School*\u0026rdquo; OR \u0026ldquo;Medical Education\u0026rdquo; Medical Curriculum\u0026rdquo;)\u003c/p\u003e\n\u003cp\u003eAND\u003c/p\u003e\n\u003cp\u003e(\u0026ldquo;Echocardiography\u0026rdquo; OR \u0026ldquo;Echo\u0026rdquo; OR \u0026ldquo;FCU\u0026rdquo; OR \u0026ldquo;Focused Cardiac Ultrasound\u0026rdquo; OR \u0026ldquo;Ultrasound\u0026rdquo; OR \u0026ldquo;FOCUS\u0026rdquo; OR \u0026ldquo;POCUS\u0026rdquo; OR \u0026ldquo;Point of Care Ultrasound\u0026rdquo; OR \u0026ldquo;Sonography\u0026rdquo; OR \u0026ldquo;Ultrasonography\u0026rdquo; OR \u0026ldquo;HCU\u0026rdquo; OR \u0026ldquo;Hand Carried Ultrasound\u0026rdquo; OR \u0026ldquo;TTE\u0026rdquo; OR \u0026ldquo;Transthoracic Echocardiography\u0026rdquo;) \u003c/p\u003e\n\u003cp\u003eEach database will be searched by both keywords and relevant MESH headings were available.\u003c/p\u003e\n\u003cp\u003eAn example is displayed in Figure 1.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eStudy Records:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe exact search strategy used for each database is included as appendix 1. Search results and study records were managed through Covidence and EndNote X8. \u003c/p\u003e\n\u003cp\u003eOur process for including studies throughout the stages of Identification, screening, eligibility and inclusion followed the PRISMA flow diagram included in the results. Once duplicates were removed articles were screened by review of their title and abstract to see if they meet the basic eligibility criteria outlined above. This process was performed by one researcher applying the PICOS framework. Following this articles that passed the screening phase were reviewed for eligibility. This process involved two researchers performing the following process: For papers using a qualitative framework the CASP checklist (Appendix 2.) was be applied. To be eligible to be included both researchers will need to answer YES to questions 1 and 2 in section A. Studies that provided information on diagnostic accuracy of medical students or compare efficacy of different teaching methods in an RCT format were be included by default. For these studies the CONSORT checklist (Appendix 3.) was utilised and each paper given a score out of 30 to grade its methodological quality.\u003c/p\u003e\n\u003cp\u003eData collection was performed using a standardized tool (appendix 4). This was completed independently by two researchers and the results collated by the primary investigator.\u003c/p\u003e\n\u003cp\u003eDefinitions of all criteria and endpoints were agreed by the researchers before performing the search. \u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eOutcomes:\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eFor this review the primary endpoint of data extraction is the educational techniques used. Secondary endpoints including learning outcomes are described and compared where possible, for example diagnostic accuracy and trials directly comparing different teaching methods are analysed separately.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eThe original search produced 6700 articles in total from all databases searched. The flow of these articles through the study is outlined in the PRISMA flow diagram below (Fig. 1).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eProgram Characteristics\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eDemographics of the studies are outlined in table 1 and study characteristics are outlined in table 2. The majority of studies over the last decade have been conducted in the United States. Notably no studies have assessed the feasibility of conducting a dedicated FCU program in Australia. Our review reveals that FCU is currently being taught through all years of medical school in both undergraduate and postgraduate programs. There appears to be an increase in publications over the last decade also with the majority of studies being published since 2015.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eFurther data was collected on randomised controlled trials (RCTs) that compared educational modalities and diagnostic accuracy studies and these are outlined in tables 3 and 4.\u003c/p\u003e\n\u003cp\u003eDespite calls from many authors to improve efficiency and scalability of studies the predominant teaching methods are still didactic lectures and small group teaching of practical skills. To answer our research question, we reviewed alternative methods of delivering teaching for their efficiency and scalability. Very few papers provided information on the costs of the programs and so this analysis was abandoned.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFlipped Classroom\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll phases of learning FCU including image acquisition, image interpretation and integration of findings into clinical practice require the assimilation of theoretical knowledge by the learner. The practice of FCU requires an understanding of the physics involved in sound transmission, the electronics and software utilised in image formation along with knowledge of the anatomy, physiology and pathophysiology of the heart. Thus before learning this practical skill there is a requirement for significant knowledge transfer to the novice practitioner(10). The flipped classroom model of providing online content to learners prior to them attending for practical teaching now appears to be widely utilised to decrease face to face time with 39.2% of studies describing this method.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eSmall Group teaching\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eTeaching image acquisition in FCU is time-consuming and labor-intensive and previously described methods necessitate teaching in small groups(11) with a requirement for many hours of teacher time. Currently the expanding need for skilled educators occurs in conjunction with increasing clinical school class sizes which poses additional challenges.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eHands-on courses in image acquisition are demanding on faculty, most of whom are involved in busy practices and other research activities. Integration of this new modality then poses a difficult problem for medical schools that already provide full schedules to students.\u003c/p\u003e\n\u003cp\u003eCurrently the most common type of teacher for delivering this content remains doctors who are without doubt the most expensive tutor available despite alternatives existing. Other studies have utilised sonographer and peer mentoring as quantified in table 2.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAlternatives to practicing on patients\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAs sourcing sufficient patients or models is often difficult, simulators have been identified as an effective method of teaching larger cohorts. Simulators lend themselves to independent practice by Novice FCU practitioners because they are readily available, avoid consent issues and provide a standardised learning experience. Peer scanning then has also been identified as method of providing high fidelity simulated patients for practice.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eIntegration with existing programs\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAnother approach to produce efficiencies in FCU education is by integrating the teaching of FCU with other existing programs including anatomy, physiology and clinical skills. Many authors have proposed that the already busy curriculums of medical school pose a significant barrier to the introduction of new course material. If FCU could be introduced without detriment to or perhaps even to the benefit of other programs, then this would represent an efficiency in itself.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResearch Methodology\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAs described in table 2 the majority of research in this field is observational or qualitative. Whilst these studies are still useful in identifying potentially efficient methods they do not offer concrete data on which methods are the most effective or efficient. Only 11 studies compared teaching methods in the context of a randomised controlled trial and only 13 produced information that could be used to assess the diagnostic accuracy of the learners at the end of the teaching program.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe most common methods for assessing MS after receiving FCU teaching were written tests or performance on objective standardised clinical exams (OSCEs) and this was uniformly the case in the RCTs identified. For diagnostic accuracy studies student FCU results were usually compared to formal TTE or Cardiologist obtained FCU images. Some studies had experts review the images obtained by the students as a comparator.\u0026nbsp;\u003c/p\u003e"},{"header":"Discussion","content":"\u003cdiv id=\"Sec17\" class=\"Section2\"\u003e\u003ch2\u003eProgram characteristics\u003c/h2\u003e\u003cp\u003eYear of medical School\u003c/p\u003e\u003cp\u003eTwo studies directly assessed whether the timing of FCU training affected Learning outcomes(\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e) Byrne\u0026rsquo;s study of 2019 assessed whether year of medical school affected learners\u0026rsquo; ability to learn FCU by dividing them into early and late clinical years of medical school. In Switzerland this relates to years 3 and 4 for vs 5 and 6 of medical school. This study demonstrated that students who were more advanced in their training performed better than students in their early years on written assessments. No difference was found however, when assessing the clinical skill of performing FCU. The difference in written skill may be confounded by other knowledge gained during medical school and the authors concluded that learning the practical skill of FCU can be incorporated at whatever level is most convenient to training(\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e).\u003c/p\u003e\u003cp\u003eCawthorn 2014(\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e) assessed the ability of first and third year medical students to perform FCU and retain knowledge regarding it. They demonstrated that both groups could be taught FCU knowledge and skills. Whilst not directly compared the third-year students in this study showed greater improvement in both knowledge and skills and again the authors attributed this to greater background knowledge gained during other aspects of medical school.\u003c/p\u003e\u003cp\u003eIn summary FCU is currently being taught in all phases of medical school with no clear evidence of benefit for a particular time point but an indication that students in later years might benefit from the additional experience they have gained in other studies. It may be that the best strategy is to begin early to assist in incorporating more teaching over several years without affecting other curricula adversely. Several studies have described longitudinal programs and these will be discussed separately.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec18\" class=\"Section2\"\u003e\u003ch2\u003eOnline content\u003c/h2\u003e\u003cp\u003eIn an effort to decrease face to face time for both students and teachers many programs have converted all or a component of their didactic teaching to online content. This may take the form of written content, recorded video lectures, online image libraries or even practical instructional videos. Details of the online content described in the studies vary from brief outlines to detailed descriptions of structured programs. For example the system developed by Beaton(\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e) utilised on-line image libraries, instructional modules and feedback via interactive quizzes to cover both knowledge transfer and image interpretation (\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e). Proponents of online systems emphasise the benefits of asynchronous learning completed at the learner\u0026rsquo;s convenience thereby enhancing integration with existing busy medical courses.\u003c/p\u003e\u003cp\u003eNovel approaches to delivering online content include the use of social media(\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e). Bahner 2012 demonstrated that the push technology of Facebook and twitter could be used to deliver online content to learners on a daily basis which received good feedback on qualitative surveys. Hempel conducted a randomized controlled trial evaluating the effectiveness of a \"sandwich e-learning\" model for point-of-care ultrasound (POCUS) training among 62 medical students. This model combined pre-course e-learning, a one-day hands-on course, and post-course social media\u0026ndash;based learning via Facebook. Four groups were compared, varying in access to pre- and/or post-course e-learning. After six weeks, knowledge retention was similar across all groups, but students with post-course social media access reported greater satisfaction. The study supports the feasibility and acceptability of integrating social media into blended ultrasound education, without compromising knowledge retention.\u003c/p\u003e\u003cp\u003eThere are several studies directly comparing face to face teaching with online programs. Cawthorn\u0026rsquo;s study of 2013 compared face to face didactic teaching with electronic modules and showed digital content was equivalent to didactic teaching in knowledge transfer for 3rd year medical students. This finding was replicated by Florescu 2014 (\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e) who found a video podcast produced equivalent learning outcomes to a face-to-face lecture. Hempel 2014(\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e) found that online teaching was superior to face to face teaching for knowledge acquisition and no different for practical skills acquisition.\u003c/p\u003e\u003cp\u003eGiven the perennial nature of online resources and the benefits from asynchronous learning form the flipped classroom model, online learning is likely to be a significant feature of future FCU teaching programs. To date most models of teaching involve face to face contact at some point usually during hands on small group teaching. Indeed, the study by Cawthorn et al(\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e) that attempted a fully self-directed course found that outcomes were not as good as with some face-to-face teaching. Future research here may need to focus on defining what the minimum instructor time that is required and when this time is best utilised.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec19\" class=\"Section2\"\u003e\u003ch2\u003eSmall group hands on teaching\u003c/h2\u003e\u003cp\u003eIn the traditional cardiology format of performing TTE a highly trained sonographer acquires the images which are then interpreted by a cardiologist. This system recognises the independent expert skill sets of image acquisition and image interpretation held by the two craft groups. In the educational setting then it makes sense to utilise the specific expertise of both groups also. Whilst many programs have demonstrated the efficacy of using sonographers to provide teaching there have been no trials comparing sonographers to other expert staff to teach image acquisition. Given Sonographers represent a significant cost saving in the delivery of image acquisition training their integration into curriculum warrants further assessment in comparative trials.\u003c/p\u003e\u003cp\u003eMost trials utilise ratios of between 1 to 3 and 1 to 5 to deliver practical hands-on training. This Teaching has been delivered by various groups of doctors including emergency physicians, Intensivists, cardiologist and anaesthetists as well as by trained sonographers without comparative trials that might determine a clear benefit of any particular group.\u003c/p\u003e\u003cp\u003eTwo authors have demonstrated the effectiveness of using digital solutions to increase teaching ratios and thereby produce efficiencies. Utilising a large screen and multiple small screens at each station of students a trial by (\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e) Evans demonstrated the effectiveness of a 1:80 ratio of instructors to students. However qualitative feedback from students revealed they wanted closer instruction.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec20\" class=\"Section2\"\u003e\u003ch2\u003ePeer Mentoring\u003c/h2\u003e\u003cp\u003eIdentifying sufficient numbers of experienced instructors to teach large cohorts is difficult and represents a barrier to scalability over and above cost. To overcome this several authors have utilised previously trained medical students to assist in delivering teaching to subsequent cohorts(\u003cspan additionalcitationids=\"CR23\" citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e). This concept of peer mentoring is not new to medical school and has been adopted widely in the delivery of other curriculae(\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e).\u003c/p\u003e\u003cp\u003ePeer mentors can be identified within a cohort of students receiving a standard teaching program or alternatively some authors have taken the approach of providing specific training in teaching FCU to smaller groups of medical students who then go on to teach a larger cohort. These students have either been identified as being particularly skilled or self-selected from the cohort. Peer mentors have been utilised for both didactic knowledge delivery and for teaching practical skills. However, as image acquisition requires the most face-to-face time it is the component with the most efficiency gains when utilising peer mentoring.\u003c/p\u003e\u003cp\u003eThe effectiveness of peer mentoring has been assessed in trials comparing it to teaching by experts with mixed results. In a trial comparing teaching by experts to teaching by trained MS it was (\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e)demonstrated that MS taught by peers showed significantly better FCU skills than expert trained peers. The authors hypothesised that the student teachers found it easier to relate to the difficulties their students encountered and more closely remembered their strategies for overcoming them. Likewise Ahn (\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e) found that senior peer instructors received equivalent scores to instructors from students who received their teaching. Conversely the trial by Kuhl et al of 2012 demonstrated that whilst peer teachers could provide teaching that objectively improved MS skill in FCU, this teaching was inferior to that provided by experts. From a qualitative perspective Gradl-Dietsch 2018(\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e) demonstrated that whilst peer teaching could deliver equivalent educational outcomes on objective measures when asked in qualitative surveys, students would have preferred expert mentors to peer teaching. This is contrasted to the findings of Dickerson (\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e) and Fu (\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e) who found overwhelming support for peer teaching from MS who received this teaching.\u003c/p\u003e\u003cp\u003eThe heterogeneity in outcomes using peer scanning may relate to the training and selection of peer tutors. Whilst this method holds promise for improving scalability the best method of achieving this remains elusive.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec21\" class=\"Section2\"\u003e\u003ch2\u003ePeer Scanning\u003c/h2\u003e\u003cp\u003eSeveral studies have described using peers as live models for scanning. (\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e, \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e). The use of human models for teaching has a requirement for payment and poses a significant burden of logistics in organising models. Medical students however have demonstrated a keenness to participate as models for their peers without payment to facilitate their learning and skill acquisition. Young male medical students usually have good acoustic windows and represent ideal models for demonstrating normal anatomy with FCU. Volunteering as a model may also represent an additional exposure to teaching during the teaching program representing an auxiliary benefit to the MS model(\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e).\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec22\" class=\"Section2\"\u003e\u003ch2\u003eSimulators\u003c/h2\u003e\u003cp\u003eSeveral studies have now compared simulators to traditional human models for delivering FCU education.\u003c/p\u003e\u003cp\u003eBentley 2015 and Hempel 2020 (\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e) compared simulators to traditional teaching with human models in non-inferiority designs. In these studies there was equivalent transfer of both theoretical knowledge and practical skill. Damewood(\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e) also demonstrated that the use of a Simulator in FCU education could provide equivalent results to teaching with live models. Their group further proposed that a simulator allows more pathologies to be seen quickly though it can be argued that this can be overcome quickly with an image library. Kusenose (\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e) Compared simulator use to textbook learning for didactic teaching and found students receiving the simulator teaching hasd faster scan completion times, improved image acquisition skill and higher satisfaction.\u003c/p\u003e\u003cp\u003e The technology embedded in some simulators also provides for novel educational opportunities and simulation has been found to hold unique potential for providing feedback in two recent reviews. (\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e, \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e)Ellison(\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e) demonstrated the use of a simulator to give immediate feedback to students after image acquisition to help guide the students probe position. They argued this gives students individualised feedback specific to their need even if they are working without supervision. Whilst this study demonstrated a well-designed educational program that could be approached by students in an entirely self-directed manner unfortunately it did not test students\u0026rsquo; ability to obtain images on human subjects as an outcome. The authors propose that their basic training might precede face to face teaching with experts who could then teach more advanced skills or focus on learners who took longer to develop a basic FCU skill set. Cecilio fernandes 2020 also demonstrated that in built feedback technologies could be used for image acquisition teaching to MS. However, in this small randomised controlled trial feedback from experts proved superior to feedback from the simulator. This may be due to expert feedback adding clinical relevance and feedback in context.\u003c/p\u003e\u003cp\u003eLe (\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e) demonstrated further that Simulators assist knowledge retention when used after a formal ultrasound course. They proposed that the use of simulators as an adjunct to supervised training on live models represented an efficient option for ultrasound training. Providing open access to an ultrasound simulator might permit students to maintain their skills without further supervised training. Jensen (\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e) examined the effectiveness of simulation-based training using a mastery learning approach. In this prospective study, 25 medical students with no prior ultrasound experience trained on a virtual-reality simulator until they reached a predefined expert-level performance. Twenty-three participants (92%) achieved mastery within a median of 1 hour and 46 minutes. Despite attaining the competency threshold, examination efficiency (speed) continued to improve with additional training. The findings challenge volume-based training models and support individualized, competency-based ultrasound education.\u003c/p\u003e\u003cp\u003eDeiden (\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e) used a qualitative framework to explore student\u0026rsquo;s perceptions and experience with simulator based FCU education. Through focus group interview with medical students they explored themes that defined the main challenges of learning FCU with a view to improving future programs.\u003c/p\u003e\u003cp\u003eStudent responses highlighted that \u0026ldquo;play\u0026rdquo; was helpful to their learning of FCU. The student perception was that without oversight they could freely make, and then learn from, their mistake without prejudice.\u003c/p\u003e\u003cp\u003eThis concept of allowing students to engage with the simulator in a self-directed manner may be a useful component of future simulator courses. The idea of integrating deliberate discussion of errors as adjuncts to self-directed simulator teaching may also improve knowledge acquisition as it utilises a logical approach to dissecting errors. In summary whilst the best methods of utilising simulators in efficient FCU teaching programs has not been defined there is clear potential for scalable solutions utilising them.\u003c/p\u003e\u003cdiv id=\"Sec23\" class=\"Section3\"\u003e\u003ch2\u003eSelf- Directed Practice\u003c/h2\u003e\u003cp\u003eAllowing students time to practice independently either with a simulator or US and a human model or patient may be an efficient method of increasing student experience with ultrasound as it promotes self-paced learning and provides the opportunity to learn through repletion and practice. Studies (\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e, \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e) have described this usually incorporating self-directed practice at some point in a program with other supervision or feedback. This process Can be assisted with written handouts describing lessons plans or specific educational goals for self-directed sessions.\u003c/p\u003e\u003cp\u003eFuture research may shed light on the balance between supervised and self-directed practice as it may be that self-directed practice is more beneficial when preceded by direct supervision. Also the best mechanisms of giving students guidance and feedback during self-directed practice are not yet defined.\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv id=\"Sec24\" class=\"Section2\"\u003e\u003ch2\u003eRemote Teaching\u003c/h2\u003e\u003cp\u003eRussell(\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e) conducted a pilot randomized study to assess the feasibility of teaching cardiac ultrasound remotely using Google Glass telementoring. The study demonstrated that telementoring via wearable technology is a viable alternative to in-person instruction for novice ultrasound users.\u003c/p\u003e\u003cdiv id=\"Sec25\" class=\"Section3\"\u003e\u003ch2\u003eCompetition\u003c/h2\u003e\u003cp\u003eSeveral studies have described the (\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e) (\u003cspan additionalcitationids=\"CR44 CR45\" citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e46\u003c/span\u003e)gamification of ultrasound teaching or the introduction of competition to motivate asynchronous self-study of ultrasound (US), qualitative evidence from these studies suggests this may be a cost effective way to improve engagement.\u003c/p\u003e\u003cp\u003e\u003cb\u003eIntegration with existing medical school teaching.\u003c/b\u003e\u003c/p\u003e\u003cp\u003eFor the following sections only studies that involved the hands-on teaching of FCU were included. Specifically, studies that described teachers utilising ultrasound to demonstrate concepts without teaching students themselves to acquire images were excluded.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec26\" class=\"Section3\"\u003e\u003ch2\u003eTeaching anatomy\u003c/h2\u003e\u003cp\u003eTo those who teach FCU the auxiliary benefits of increasing students\u0026rsquo; knowledge of anatomy are obvious and several recent studies have demonstrated this.\u003c/p\u003e\u003cp\u003eHammoudi (\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e) demonstrated integration of ultrasound to a cohort of 330 medical students using existing faculty resources and the addition of ultrasound machines. The course received excellent qualitative feedback a feature consistent in other studies using qualitative assessment.\u003c/p\u003e\u003cp\u003eIn the quantitative arena Canty(\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e) demonstrated that an ultrasound simulator could be used to teach cardiac anatomy with effectiveness equivalent to traditional cadaveric based teaching. The efficacy of ultrasound based anatomy teaching was further demonstrated by Kondrashov(\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e) with improved scores on an anatomy exam with a before and after study design.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec27\" class=\"Section3\"\u003e\u003ch2\u003eIntegration with existing clinical skills teaching\u003c/h2\u003e\u003cp\u003eMost clinical exposure is in ED and ICU(\u003cspan additionalcitationids=\"CR51\" citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e) and programs can be set up with minimal additional resource by integrating with existing clinical services in these areas which ordinarily have access to point of care ultrasound devices in a contemporary clinical context. Fu(\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e) performed qualitative assessments on learners experience in which ED and ICU were identified as exceptional clinical environments for learning FCU. The authors discuss the idea that this clinical context allows the beginning of integration into clinical practice. Notably in our review very few studies discuss how they teach the final step of integrating US findings into clinical practice. Other clinical settings that have been investigated include final year anaesthesia selective(\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e53\u003c/span\u003e) and a radiology elective.(\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e)\u003c/p\u003e\u003c/div\u003e\u003c/div\u003e\u003cdiv id=\"Sec28\" class=\"Section2\"\u003e\u003ch2\u003eImproving Clinical Skills\u003c/h2\u003e\u003cp\u003eWhen integrated with traditional clinical skills FCU teaching has been reported to improve bedside acumen. Dinh(\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e) and Liu(\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e) demonstrated that implementing FCU into a clinical skills curriculum for MS was feasible and could improve student usual beside skills as measured on OSCE\u0026rsquo;s that formed part of academic assessment.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec29\" class=\"Section2\"\u003e\u003ch2\u003eLongitudinal programs\u003c/h2\u003e\u003cp\u003eSeveral longitudinal programs already exist(\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan additionalcitationids=\"CR58\" citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e) that range for one year or longer in which FCU skills are integrated with existing programs including anatomy, physiology and clinical skills. These programs build FCU skills on foundational anatomy and ultrasound knowledge gained in earlier years without interrupting existing teaching.\u003c/p\u003e\u003cp\u003eRapaport 2019 identified that FCU image acquisition skills deteriorate over time when not used. As such these integrated programs may well benefit from the continuous exposure of learners to ultrasound over subsequent years.\u003c/p\u003e\u003cp\u003eMethodological Considerations\u003c/p\u003e\u003cp\u003eMany studies have incorporated a bespoke FCU based OSCE to assess the effectiveness of their teaching intervention. For instance all of the RCTs identified used their own MCQ or OSCE preventing further comparison between trials. These OSCEs are usually a qualitative assessment of images and the process of their acquisition which has the advantage of being rapid but often has a subjective component. Whilst these can assess the transfer of theoretical knowledge and basic procedural skill they do not assess the student\u0026rsquo;s ability to perform FCU in the real world.\u003c/p\u003e\u003cp\u003eSome studies have developed detailed image quality analysis tools as part of an OSCE process solely for the purpose of their study. When such systems already exist this duplication of effort may impede the progress of future research.\u003c/p\u003e\u003cp\u003eA more objective measure is the use of a validated image quality score as described in 14 studies in this review. The use of an objective image scoring system allows specific analysis of a student\u0026rsquo;s skills in image acquisition. This then allows assessment of the effectiveness of different educational modalities particularly when the scoring system allows quantitative assessment over a broad range of image quality. Image quality scoring Systems that only use categorical analysis of image quality do not allow finer analysis of image quality particularly at the higher end of quality. Ie systems that simply grade whether depth and gain have been adjusted adequately or whether a particular structure can be identified and labelled do not have the same discrimination as systems that analyse whether all the anatomical structures usually identified in a particular echo view can be identified.\u003c/p\u003e\u003cp\u003eWhere simulators are employed it is possible to assess a learner\u0026rsquo;s image by analysing their probe position and angle relative to an ideal view. Hence other authors have sought to uses in built technology in simulators to assess students(\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e, \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e60\u003c/span\u003e).\u003c/p\u003e\u003cp\u003eThis has the advantage of rapid computer assisted analysis of image quality but the disadvantage of not measuring real world conditions that exist due to the variability in human anatomy between patients and even models. Whilst image libraries can be used for image interpretation this does not account for the cognitive load associated with performing and interpreting the scan simultaneously. The effects of cognitive load are likely to be more marked with novice learners.\u003c/p\u003e\u003c/div\u003e\n\u003ch3\u003eDiagnostic Accuracy\u003c/h3\u003e\n\u003cp\u003eDiagnostic accuracy studies tended to have a smaller number of students with an average class size for diagnostic accuracy studies of 16.4 compared with the average a class size of 89.2 for other studies. This presumably relates to the increased burden of performing a formal diagnostic accuracy study but reveals that accuracy of large cohorts of students learning FCU has not been assessed.\u003c/p\u003e\u003cp\u003ePanoulas 2013 \u0026ndash; showed that brief intervention improved bedside assessment over and above history and examination. The aim of this study was to examine whether students could improve their diagnostic accuracy at the bedside with the assistance of FCU. This is consistent with a pilot study by Parks 2015 suggesting that medical learners new to FCU, the addition of the \u0026ldquo;ACES PoCUS\u0026rdquo; protocol to standard clinical assessment improved diagnostic accuracy. This is a fundamental question of the benchmark of FCU in this setting. Is the aim of teaching FCU to improve bedside skills with or without the use of ultrasound or should FCU be compared to TTE or simply to existing bedside clinical skills?\u003c/p\u003e\u003cp\u003eThe latter is poorly defined in terms of diagnostic accuracy and has significant heterogeneity in quality between institutions. The former is a standardised diagnostic test with known accuracy which assists in comparative studies but exists separate to usual bedside skills.\u003c/p\u003e\u003cp\u003eKnowing the true diagnostic accuracy of FCU would be enormously useful in deciding where it fits into a diagnostic algorithms and further teaching of bedside skills. As this has not been done formally for traditional bedside skills a Bayesian analysis of diagnostic certainty utilising pre and post test probabilities would be a new endeavour for FCU researchers. These studies may set the bench mark for efficacy of teaching with future studies trying to replicate findings with less resources or greater numbers of students.\u003c/p\u003e\u003cdiv id=\"Sec31\" class=\"Section2\"\u003e\u003ch2\u003eCosts\u003c/h2\u003e\u003cp\u003eFew studies give detailed information on the cost of their program. It is often unclear whether resources are shared, existing or bought as new for the project. It is common for researchers to be delivering the educational material in a voluntary capacity often for the secondary gain of generating the research. This is an excellent motivator whilst generating research outcomes it belies the fact the ongoing provision of teaching will have associated costs(\u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e61\u003c/span\u003e)\u003c/p\u003e\u003cp\u003eFor instance a feasibility study by Gogalnicaeu (\u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e61\u003c/span\u003e) quoted their cost as minimal as the 5 US machines utilised were donated by industry for the project and all faculty participated pro bono. Notably they benchmark costs of a 1 day commercial course in the UK between \u0026pound;250 and \u0026pound;400 per student. These courses are available to undergraduates.\u003c/p\u003e\u003c/div\u003e\u003cdiv id=\"Sec32\" class=\"Section2\"\u003e\u003ch2\u003eFuture Research\u003c/h2\u003e\u003cp\u003eImage quality scoring systems that are previously validated hold the potential to set benchmarks for teaching image acquisition in FCU and ongoing comparison between studies. Although assessing image acquisition and interpretation independently has advantages for analysing the different components of a teaching program unless they are analysed concurrently the results may not reflect student\u0026rsquo;s future performance in real world conditions.\u003c/p\u003e\u003cp\u003eHence studies targeting diagnostic accuracy with larger cohorts are warranted. Here measures of agreement should be considered. Whilst sensitivity and specificity are immediately recognisable to most clinicians, they may not be the best measures of agreement for these studies. The kappa statistic has been used with good effect to convey chance corrected agreement that takes into account both the prevalence of the pathology and also the size of the sample.\u003c/p\u003e\u003cp\u003eThere remains a deficit of randomised controlled trials particularly with larger cohorts to define the best methods to teach the large cohorts that exist in most medical schools.\u003c/p\u003e\u003cp\u003eFinally, more high quality diagnostic accuracy studies are needed to determine the true accuracy of medical students after receiving this teaching.\u003c/p\u003e\u003c/div\u003e"},{"header":"Conclusion","content":"\u003cp\u003e Our review reveals that research in MS FCU teaching is being led by the US and appears to be increasing in volume. Further this research has not yet commenced in Australia. Current evidence suggests that teaching can occur effectively in any year of medical school.\u003c/p\u003e\u003cp\u003e This systematic review has identified a number of educational modalities that have the potential to contribute to increasingly efficient educational programs in FCU. For instance the flipped classroom model now appears to be defined as the most efficient method of knowledge transfer and image interpretation. However, the methodological limitations of the majority of studies means that further research will be required to define the most efficient methods of teaching image acquisition and integration into clinical practice.\u003c/p\u003e\u003cp\u003eCurrently comparison of educational modalities is hampered by the outcome measures used to assess most programs. Written tests whilst useful in assessing theoretical knowledge do not assess a student\u0026rsquo;s skill level in performing FCU. In this regard objective image quality scoring tools appear to hold the most promise. Widespread use of these tools would allow the comparison between different studies and of educational programs as they are adapted over time.\u003c/p\u003e\u003cp\u003eThere is a paucity of high quality evidence targeting diagnostic accuracy achieved with FCU by MS. Diagnostic accuracy studies to date have been small and lack generalisability. The use of formal TTE and the kappa statistic to assess for agreements seems to hold promise in the future but trials will need to include larger numbers of students to determine generalisability.\u003c/p\u003e\u003cp\u003eFurther investigation is warranted to evaluate the feasibility and effects of specific educational modalities for teaching image acquisition, the use of simulators, self-directed practice, engaging peers in scanning and sonographers as educators.\u003c/p\u003e\u003cp\u003eThe flipped classroom has now proven to be highly acceptable to students and overcomes many of the barriers related to crowded curricula and student timetables. As a perennial resource is may also decrease the annual requirement for face-to-face teacher time. Simulators may provide efficiencies by decreasing the burden on patients or the cost of models whilst maximising the time students can spend practicing and minimising time spent consenting patients. Peer scanning could be the ultimate high-fidelity simulator and has again been shown to be quite acceptable to students.\u003c/p\u003e\u003cp\u003eAs programs minimise teacher face-to-face time the ideal amount of clinician interaction with the students remains to be determined as does which clinicians should be involved. As sonographers are the experts in image acquisition in cardiology they may represent a potentially cost effective solution.\u003c/p\u003e\u003cp\u003eIn terms of scalability the use of echo simulator appears to hold the greatest potential for teaching image acquisition. The early success of trials that utilise either in built feedback mechanisms in the simulators or additional teaching materials that facilitate self-directed learning certainly holds promise for defining further scalable and efficient solutions here.\u003c/p\u003e\u003cp\u003eIt is possible that integration of ultrasound into existing curricula may be an efficient way of teaching. From the perspective of FCU teaching it is likely that learners benefit from the consolidation of skills over time. There also remains a deficit in the research of how FCU skills are integrated into clinical practice. It may be that until diagnostic accuracy is defined in this group there remains a reluctance to incorporate FCU findings into clinical assessment. Conversely where FCU skill is defined, MS may find themselves leading team interaction within assigned teams during ward rounds and other clinical duties.\u003c/p\u003e\u003cp\u003eIn conclusion further high-quality research is required to define the feasibility and the most efficient methods of teaching FCU to MS. A multi-modal teaching approach involving the flipped classroom, simulators, peer scanning, sonographers as teachers and finally integrated clinical placements to consolidate skills may promote integration and translation of FCU skills into clinical practice.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eHuman ethics and Consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e\n\u003cp\u003eAs a systematic review article no participants were directly recruited for this research.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNo funding was obtained to complete this research\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eClinical trial number\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eBahner DP, Goldman E, Way D, Royall NA, Liu YT. The state of ultrasound education in U.S. medical schools: results of a national survey. Acad Med. 2014;89(12):1681-6.\u003c/li\u003e\n\u003cli\u003eDecara JM, Kirkpatrick JN, Spencer KT, Ward RP, Kasza K, Furlong K, et al. Use of hand-carried ultrasound devices to augment the accuracy of medical student bedside cardiac diagnoses. J Am Soc Echocardiogr. 2005;18(3):257-63.\u003c/li\u003e\n\u003cli\u003e\u0026lt;Galderisi 2010.pdf\u0026gt;.\u003c/li\u003e\n\u003cli\u003eTestuz A, Muller H, Keller PF, Meyer P, Stampfli T, Sekoranja L, et al. Diagnostic accuracy of pocket-size handheld echocardiographs used by cardiologists in the acute care setting. Eur Heart J Cardiovasc Imaging. 2013;14(1):38-42.\u003c/li\u003e\n\u003cli\u003eChamsi-Pasha MA, Sengupta PP, Zoghbi WA. Handheld Echocardiography: Current State and Future Perspectives. Circulation. 2017;136(22):2178-88.\u003c/li\u003e\n\u003cli\u003eLucas BP, Candotti C, Margeta B, Evans AT, Mba B, Baru J, et al. 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Eur J Trauma Emerg Surg. 2018;44(1):143-52.\u003c/li\u003e\n\u003cli\u003e\u0026lt;dickerson 2016 peer assisted.pdf\u0026gt;.\u003c/li\u003e\n\u003cli\u003eFu JY, Krause C, Krause R, McCoy J, Schindler A, Udrea DS, et al. Integration of Point-of-Care Ultrasound Training into Undergraduate Medical Curricula--A Perspective from Medical Students. J Med Educ Curric Dev. 2016;3.\u003c/li\u003e\n\u003cli\u003eAbu-Zidan FM, Cevik AA. Kunafa knife and play dough is an efficient and cheap simulator to teach diagnostic Point-of-Care Ultrasound (POCUS). World J Emerg Surg. 2019;14:1.\u003c/li\u003e\n\u003cli\u003eBentley S, Mudan G, Strother C, Wong N. Are Live Ultrasound Models Replaceable? Traditional versus Simulated Education Module for FAST Exam. Western Journal of Emergency Medicine: Integrating Emergency Care with Population Health. 2015;16(6):818-22.\u003c/li\u003e\n\u003cli\u003eDamewood S, Jeanmonod D, Cadigan B. 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Focused cardiac ultrasound training in medical students: Using an independent, simulator-based curriculum to objectively measure skill acquisition and learning curve. Echocardiography. 2020;37(4):491-6.\u003c/li\u003e\n\u003cli\u003eLe CK, Lewis J, Steinmetz P, Dyachenko A, Oleskevich S. The Use of Ultrasound Simulators to Strengthen Scanning Skills in Medical Students: A Randomized Controlled Trial. J Ultrasound Med. 2019;38(5):1249-57.\u003c/li\u003e\n\u003cli\u003eJensen JK, Dyre L, Jorgensen ME, Andreasen LA, Tolsgaard MG. Simulation-based point-of-care ultrasound training: a matter of competency rather than volume. Acta Anaesthesiol Scand. 2018;62(6):811-9.\u003c/li\u003e\n\u003cli\u003eKobal SL, Lior Y, Ben-Sasson A, Liel-Cohen N, Galante O, Fuchs L. The feasibility and efficacy of implementing a focused cardiac ultrasound course into a medical school curriculum. BMC Med Educ. 2017;17(1):94.\u003c/li\u003e\n\u003cli\u003eMackay FD, Zhou F, Lewis D, Fraser J, Atkinson PR. Can You Teach Yourself Point-of-care Ultrasound to a Level of Clinical Competency? Evaluation of a Self-directed Simulation-based Training Program. Cureus. 2018;10(9):e3320.\u003c/li\u003e\n\u003cli\u003eRussell PM, Mallin M, Youngquist ST, Cotton J, Aboul-Hosn N, Dawson M. First \u0026quot;glass\u0026quot; education: telementored cardiac ultrasonography using Google Glass- a pilot study. Acad Emerg Med. 2014;21(11):1297-9.\u003c/li\u003e\n\u003cli\u003eBoulger C, Liu RB, De Portu G, Theyyunni N, Lewis M, Lewiss RE, et al. A National Point-of-Care Ultrasound Competition for Medical Students. Journal of Ultrasound in Medicine. 2019;38(1):253-8.\u003c/li\u003e\n\u003cli\u003eAmini R, Stolz LA, Hernandez NC, Gaskin K, Baker N, Sanders AB, et al. Sonography and hypotension: a change to critical problem solving in undergraduate medical education. Adv Med Educ Pract. 2016;7:7-13.\u003c/li\u003e\n\u003cli\u003eBahner DP, Royall NA. Advanced ultrasound training for fourth-year medical students: a novel training program at The Ohio State University College of Medicine. Acad Med. 2013;88(2):206-13.\u003c/li\u003e\n\u003cli\u003eBoulger C, Liu RB, De Portu G, Theyyunni N, Lewis M, Lewiss RE, et al. A National Point-of-Care Ultrasound Competition for Medical Students. J Ultrasound Med. 2019;38(1):253-8.\u003c/li\u003e\n\u003cli\u003eAmini R, Stolz LA, Gross A, O\u0026apos;Brien K, Panchal AR, Reilly K, et al. Theme-based teaching of point-of-care ultrasound in undergraduate medical education. Intern Emerg Med. 2015;10(5):613-8.\u003c/li\u003e\n\u003cli\u003eHammoudi N, Arangalage D, Boubrit L, Renaud MC, Isnard R, Collet JP, et al. Ultrasound-based teaching of cardiac anatomy and physiology to undergraduate medical students. Arch Cardiovasc Dis. 2013;106(10):487-91.\u003c/li\u003e\n\u003cli\u003eCanty DJ, Hayes JA, Story DA, Royse CF. Ultrasound simulator-assisted teaching of cardiac anatomy to preclinical anatomy students: A pilot randomized trial of a three-hour learning exposure. Anat Sci Educ. 2015;8(1):21-30.\u003c/li\u003e\n\u003cli\u003eKondrashov P, Johnson JC, Boehm K, Rice D, Kondrashova T. Impact of the clinical ultrasound elective course on retention of anatomical knowledge by second-year medical students in preparation for board exams. Clin Anat. 2015;28(2):156-63.\u003c/li\u003e\n\u003cli\u003eBahner DP, Royall NA. Advanced ultrasound training for fourth-year medical students: a novel training program at The Ohio State University College of Medicine. Academic Medicine. 2013;88(2):206-13.\u003c/li\u003e\n\u003cli\u003eBlackstock U, Munson J, Szyld D. Bedside ultrasound curriculum for medical students: report of a blended learning curriculum implementation and validation. J Clin Ultrasound. 2015;43(3):139-44.\u003c/li\u003e\n\u003cli\u003eArias Felipe A, Dom\u0026eacute;nech Garc\u0026iacute;a J, S\u0026aacute;nchez los Arcos I, Luordo D, Garc\u0026iacute;a S\u0026aacute;nchez FJ, Villanueva Mart\u0026iacute;nez J, et al. Teaching the basics of echocardiography in the undergraduate: Students as mentors. Revista Cl\u0026iacute;nica Espa\u0026ntilde;ola (English Edition). 2017;217(5):245-51.\u003c/li\u003e\n\u003cli\u003eHo AM, Critchley LA, Leung JY, Kan PK, Au SS, Ng SK, et al. Introducing Final-Year Medical Students to Pocket-Sized Ultrasound Imaging: Teaching Transthoracic Echocardiography on a 2-Week Anesthesia Rotation. Teach Learn Med. 2015;27(3):307-13.\u003c/li\u003e\n\u003cli\u003eLimchareon S, Asawaworarit N, Klinwichit W, Dinchuthai P. Development of the ultrasonography learning model for undergraduate medical students: A case study of the Faculty of Medicine, Burapha University. J Chin Med Assoc. 2016;79(8):445-9.\u003c/li\u003e\n\u003cli\u003eDinh VA, Frederick J, Bartos R, Shankel TM, Werner L. Effects of ultrasound implementation on physical examination learning and teaching during the first year of medical education. J Ultrasound Med. 2015;34(1):43-50.\u003c/li\u003e\n\u003cli\u003eLiu RB, Suwondo DN, Donroe JH, Encandela JA, Weisenthal KS, Moore CL. Point-of-Care Ultrasound: Does it Affect Scores on Standardized Assessment Tests Used Within the Preclinical Curriculum? J Ultrasound Med. 2019;38(2):433-40.\u003c/li\u003e\n\u003cli\u003eMinardi J, Ressetar H, Foreman T, Craig K, Sharon M, Bassler J, et al. Longitudinal Ultrasound Curriculum Incorporation at West Virginia University School of Medicine: A Description and Graduating Students\u0026apos; Perceptions. J Ultrasound Med. 2019;38(1):63-72.\u003c/li\u003e\n\u003cli\u003eNelson BP, Hojsak J, Dei Rossi E, Karani R, Narula J. Seeing Is Believing: Evaluating a Point-of-Care Ultrasound Curriculum for 1st-Year Medical Students. Teach Learn Med. 2017;29(1):85-92.\u003c/li\u003e\n\u003cli\u003eHoppmann RA, Rao VV, Bell F, Poston MB, Howe DB, Riffle S, et al. The evolution of an integrated ultrasound curriculum (iUSC) for medical students: 9-year experience. Crit Ultrasound J. 2015;7(1):18.\u003c/li\u003e\n\u003cli\u003eJensen JK, Dyre L, Jorgensen ME, Andreasen LA, Tolsgaard MG. Collecting Validity Evidence for Simulation-Based Assessment of Point-of-Care Ultrasound Skills. J Ultrasound Med. 2017;36(12):2475-83.\u003c/li\u003e\n\u003cli\u003eGogalniceanu P, Sheena Y, Kashef E, Purkayastha S, Darzi A, Paraskeva P. Is basic emergency ultrasound training feasible as part of standard undergraduate medical education? J Surg Educ. 2010;67(3):152-6.\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1 to 4 are available in the Supplementary Files section\u003c/p"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-7521606/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-7521606/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003eBackground\u003c/strong\u003e\u003cbr\u003e\nFocused Cardiac Ultrasound (FCU) is increasingly incorporated into medical curricula, yet widespread adoption is limited by faculty availability, teaching resources, and curriculum overload. This review aimed to identify and evaluate current educational strategies for teaching FCU to medical students, with a focus on efficiency, scalability, and diagnostic outcomes.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eMethods\u003c/strong\u003e\u003cbr\u003e\nWe conducted a systematic review following PRISMA guidelines. Eight databases were searched including PubMed, MEDLINE, Scopus, EMBASE, Web of Science, Cochrane Central, Google Scholar, and clinical trial registries. Eligible studies included those involving undergraduate or postgraduate medical students learning FCU, reporting on teaching methods, learning outcomes, diagnostic accuracy, or resource use. Data were extracted independently by two reviewers. Risk of bias was assessed using the CASP checklist for qualitative studies, STARD for diagnostic accuracy, and CONSORT scoring for randomized controlled trials.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eResults\u003c/strong\u003e\u003cbr\u003e\nFrom 6,700 records, 99 studies were included. Teaching methods included didactic sessions (73%), hands-on practicals (85%), flipped classrooms (39%), simulation (23%), peer mentoring (12%), and self-directed practice (18%). Eleven randomized controlled trials compared different modalities; simulation and online learning were frequently found to be non-inferior to traditional teaching. Simulators and flipped classrooms were associated with increased scalability and reduced faculty time. Peer-assisted learning and curricular integration showed promise, but evidence remains limited. Only 13 studies assessed diagnostic accuracy, with small sample sizes and varied outcome measures. Objective image quality scoring tools were used in 14 studies and may facilitate future standardization.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConclusions\u003c/strong\u003e\u003cbr\u003e\nEducational strategies such as flipped classrooms, simulation, and peer teaching show potential for scalable FCU education in medical schools. However, methodological heterogeneity and limited high-quality comparative studies restrict firm conclusions. Larger, well-designed trials and diagnostic accuracy studies are needed to determine the most effective and sustainable approaches for widespread FCU integration.\u003c/p\u003e","manuscriptTitle":"Educational Methods for Teaching Focused Cardiac Ultrasound to Medical Students: A Systematic Review of Efficiency, Scalability, and Outcomes","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-10-15 16:12:23","doi":"10.21203/rs.3.rs-7521606/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"612bbf1a-1144-4765-8c4b-d39e4fbf4ac8","owner":[],"postedDate":"October 15th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2026-04-22T08:56:30+00:00","versionOfRecord":[],"versionCreatedAt":"2025-10-15 16:12:23","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-7521606","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-7521606","identity":"rs-7521606","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}