Dynamic cardiac imaging as a preclinical cardiovascular pathophysiology teaching aid: Facta non verba

Abstract

Dynamic, high-resolution imaging of functioning internal organs represents a clear, accessible, and potentially effective tool for teaching medical students preclinical pathophysiology at the basic science level. This assertion is especially true when considering the subject of cardiovascular pathology, an organ in constant motion. Color Doppler echocardiography and cardiac magnetic resonance imaging provide valuable insight into the functional consequences of cardiovascular disease. Post-processing and cine-loop technology can provide clear and concise demonstrations of specific cardiovascular disorders which can be reviewed ad infinitum. Adapting a strategy of providing dynamic examples of cardiovascular disorders can have immense benefits in teaching conceptually elusive subjects at the basic science level. A further benefit to the discipline of radiology is through increased involvement in medical student preclinical education. This is but a limited example of the large positive potential dynamic imaging can play in educating students about cardiovascular disease as well as other systems.

Introduction

The human body is a living system in a dynamic steady state. Its constituent organs are in constant motion, and many of these organ kinetics are observable at the macroscopic level. This is best exemplified by the cardiovascular system (CVS) with the heart and blood performing their respective functions in cyclic perpetuity. Even when diseased, the CVS remains in perpetual, albeit, dysfunctional motion.

It is our opinion that a dynamic organ requires dynamic imaging to fully illustrate the functional and hemodynamic consequences of cardiovascular disease (CVD) when teaching preclinical pathology and pathophysiology.

Traditionally, radiology has been included as an adjunct instructional aid when teaching pathology and anatomy. ¹ Mori et al. ² rationally argued that true cardiac anatomy and its relationship with other structures cannot be properly learned when viewed in the “Valentine” situation, which is an isolated ex vivo view typically seen in textbooks. We similarly argue that static images, radiographic or otherwise, cannot adequately convey the negative impact pathology has on both cardiac function and hemodynamics. Many radiographic modalities, namely echocardiography and cardiac magnetic resonance (CMR), are designed to image the heart and blood in motion. We, therefore, propose that these modalities should be investigated and tested with an eye to implementation as a standard part of the pathology curriculum at the basic medical science level.

This paper will focus primarily on the application of cine-loops in teaching the pathophysiology of CVD where hemodynamic and kinetic dysfunction is commonly the sequelae of pathology. The intention is not to dismiss the educational value of dynamic imaging in other organ systems but rather focus on how dynamic imaging can benefit teaching CVD at the preclinical stage.

We will discuss the benefits of dynamic imaging to the subject of CVS pathophysiology. We assert that the integration of dynamic imaging into basic science coursework is a valuable tool for enhancing the accessibility and scientific understanding of pathophysiologic processes and positively impacting the future clinical knowledge of aspiring physicians. We will also contend that our proposal will benefit radiology in terms of increasing the discipline’s role in preclinical education and introducing the technological capabilities of imaging at a preclinical stage.

Dynamic cardiac imaging

A number of modern imaging modalities are capable of safely imaging organs in motion over an extended period of time. This capacity imbues certain modalities with high temporal resolution permitting continuous real-time display of organ dynamics. ³ Specifically, this parlays into a continuous “film” of cardiac wall motion and blood flow dynamics. This capacity has immense instructional potential by demonstrating CVD pathophysiology in motion. This can aid medical students in understanding difficult concepts where organ motor dysfunction and hemodynamic compromise are the primary manifestations of cardiac disease or injury.

Both ultrasound (US) echocardiography and CMR are excellent examples of the aforementioned real-time imaging modalities. Neither rely on ionizing radiation as their mode of operation and are capable of chronologically extended investigations without endangering the patient. As such, both modalities can image multiple cardiac cycles which imbue both modalities with excellent temporal resolution. Echocardiography and CMR also demonstrate superb spatial resolution which can provide insights into cardiac morphology. This permits visualization of cardiac structural anomalies as a result of disease and what effect an anomaly may have on myocardial function and blood flow. Thus, continuous imaging coupled with first-rate anatomic resolution can exquisitely demonstrate to medical students the pathophysiologic consequences of disease. ⁴

While both echocardiography and CMR have continuous real-time attributes, modes of operation differ completely. Differences in modus operandi bestow each modality with multiple imaging techniques that can highlight specific anatomical and pathophysiologic defects. A complete discussion of the physics and imaging capabilities of both modalities is well beyond the scope of this article. Nevertheless, certain aspects of echocardiography and CMR techniques will be briefly discussed. The goal is to briefly acquaint each modality with those who may be unfamiliar and emphasize the tremendous educational potential each modality possesses.

Echocardiography can provide real-time US-generated images of heart morphology and hemodynamic function throughout the cardiac cycle.^{5 –8} Echocardiography is indicated for the evaluation of a number of cardiac structural and hemodynamic disorders. ⁹ Standard grayscale echocardiography can demonstrate valvulopathies, wall motion abnormalities, or mobile neoplasms in action. Furthermore, Doppler US provides a clear demonstration of hemodynamics. Doppler US can graphically demonstrate blood flow using a color display to represent antegrade (i.e., physiologic) and retrograde (i.e., pathophysiologic) blood flow. Combining morphologic imaging with Doppler flow imaging can act as a powerful aid in teaching the pathophysiologic consequences of structural CVS defects. For instance, Doppler color flow can dynamically display regurgitant backflow as a result of aortic valve incompetency (Figure 1). The figure was generated using select frame grabs from an online video kindly provided by Prague ICU, a web-based educational resource. ¹⁰ It displays physiologic antegrade flow through the heart chambers as red. Normally, retrograde aorta to left ventricle backflow is prevented by a competent aortic valve. Under conditions of valve incompetency, abnormal flow from the aorta to the left ventricle can be graphically displayed as a green regurgitant jet during periods when left ventricular pressure is less than aortic pressure. This dynamic depiction beautifully demonstrates the in vivo relationship between a cardiac structural malfunction, for example, valve incompetency, and its negative impact on hemodynamics.

Figure 1.

Echocardiogram with color Doppler of severe aortic regurgitation depicted in a parasternal long-axis view. This figure graphically displays the hemodynamic consequences of aortic incompetency. The figure is generated from frame grabs of an online GIF ¹⁰ and annotated using an online GIF editor. ¹¹ Frames are numbered with MS PowerPoint in the left upper corner and yellow arrows indicate the phase of the cardiac cycle relative to the bottom EKG trace. Frame 5 is annotated to provide relevant anatomical information including the left ventricle outflow tract. Frame 12 depicts the moment of AK depicted as blue. During ventricular filling, there is a simultaneous green regurgitation jet (Regurg) although the aortic valve (AoV) appears in a closed position. Frames 16–17 demonstrate a brief systolic ejection (SysEject) phase before LV pressure equalizes with systemic (LVP►◄SysP) and rapidly falls below systemic pressure permitting retrograde flow to resume which is depicted in frames 13–22. It should be noted that the frame grabs fail to fully illustrate the negative effect of AoV incompetency. The GIF, in dynamic form, demonstrates how regurgitation dominates a cardiac cycle and is only reversed for the briefest of moments during systolic ejection.

Magnetic resonance imaging or more specifically, CMR, is capable of providing a comprehensive amount of information on cardiac structure, function, and flow.^{12 –14} In addition to its spatial and temporal advantages, CMR provides excellent soft tissue contrast which can provide information on heart structure and tissue composition including the presence of abnormal tissue in the myocardial wall. Furthermore, CMR can provide multiplanar views, which can include up to all four cardiac chambers as well as the great vessels. As a result, CMR can visualize a number of pathologic conditions and their respective impact on cardiac function and hemodynamics from multiple anatomic perspectives in real time. In addition, CMR with or without contrast, offers a number of imaging sequences that can aid students by highlighting specific aspects of cardiac dysfunction. For instance, CMR can suppress blood signals to black to better display anatomic morphology and myocardial wall kinetics. ¹⁵ Black blood imaging can highlight the negative effects myocardial pathology has on pathophysiology and is indicated in such disorders as infarction, infiltration, and inflammation.^16,17 Conversely, blood can be displayed as “bright” which highlights blood flow and provides information on cardiac function. Bright blood imaging can demonstrate impaired hemodynamics such as abnormal ejection jets due to valve regurgitation or stenosis. Other hemodynamic defects readily seen with CMR also include issues such as poor contractility-induced blood stasis, flow turbulence, and septal wall defect-induced blood shunting. There is a multitude of CMR sequences available to help illustrate teaching CVD objectives. ¹⁸ Figure 2 demonstrates the functional and hemodynamic consequences of aortic valve and mitral valve regurgitation (AVR and MVR, respectively). The images were created using selected video frame grabs from an online paper by Sheth et al. ⁴ The series of frames demonstrates a dark aortic regurgitant jet present for most of the cardiac cycle. For only a brief moment does the jet cease as a result of opposing systolic ejection. The frames also demonstrate MVR, although the signs are more subtle than AVR. A mild MVR jet can be seen in a single frame as well as turbulent regurgitant flow during systolic ejection. The figure also nicely demonstrates the pulmonary congestion as a result of pulmonary vein backflow that often accompanies MVR. During systolic ejection, the pulmonary vein and deeper branch enhance brightly to indicate MV regurgitant flow is transmitted into the pulmonary circulation.

Figure 2.

Three-chamber cardiac MRI demonstrating the hemodynamic effects of both aortic and mitral regurgitation (AVR and MVR, respectively). The figure is generated from frame grabs of an online MP4 movie ⁴ and annotated using an online editor. ¹¹ Frames are numbered in the left upper corner using MS PowerPoint. Frame 2 is annotated to provide relevant anatomical information including a single pulmonary vein branch (PVB). Frame 8 demonstrates the initial moment of left ventricle systolic ejection (SysEject). The volume ejected is depicted as an enhanced ejection jet which is followed by the ascending aorta (AOA) to frame 10. Frame 10 also illustrates the hemodynamic effects of MVR. During systole, blood is visibly ejected into the left atrium. This results in retrograde turbulent flow (LATR) and is seen as a mottled black-gray pattern. The frame also demonstrates that retrograde backflow is transmitted back to the pulmonary circulation. This is indicated by the increased venous signal intensity in the PVB and deep pulmonary vein (DPVR) (n.b., one can appreciate this phenomenon when comparing frame-by-frame intensities). This phenomenon illustrates the pulmonary consequences, namely pulmonary congestion, of pulmonary backflow associated with MVR. Frame 28 shows both AVR and MVR regurgitant jets with both valves in the closed position. AVR continues into frame 32 during the atrial kick and continues until frame 50.

Presented in their respective native dynamic formats, Figures 1 and 2 embody the phrase “facta non verba,” that is, deeds not words, in regards to how dynamic imaging can succinctly illustrate cardiac pathophysiology much more eloquently than words. For a summary of the benefits of teaching with dynamic imaging, see Table 1. We hasten to suggest that the putative benefits of dynamic imaging in the classroom seem readily applicable to other organ systems, that is, pulmonary, gastrointestinal, genitourinary, and musculoskeletal.

Table 1.

Benefits of teaching cardiac pathology using dynamic imaging of a functioning organ.

Ultrasound/echocardiography	Magnetic resonance imaging/CMR
• Augmented appreciation of the cardiac cycle, internal dynamics, and simultaneous ECG	• Resolution of myocardial soft tissue
• May repeatedly review cine-loops for clarification and redundant cuing	• Multiplanar views
• Appreciation of anatomical spatial relationships in health and disease, that is, valvulopathies, wall motion abnormalities, mobile neoplasms, impact of anatomical defects on (regurgitant, retrograde) blood flow	• Variable contrast enables highlighting of morphology and wall kinetics, and pathologic conditions such as infarction, infiltration, and inflammations

Cine-loops

Echocardiography and CMR have an additional teaching advantage in the form of cine-loops. Cine-loop imaging technology permits the acquisition and storage of imaging data in digital form. ¹⁹ An imaging exam often includes multiple viewing angles, variable test conditions, multiple sequences, and native versus contrast imaging. Image sequences generally begin with a trigger signal such as an ECG. Signal triggering permits visualization of the aforementioned variables at the same point within the cardiac cycle. This allows the reviewer to thoroughly review results after the exam has been completed. This technological advantage can be also used to teach CVD pathophysiology in much the same manner that a radiologist can thoroughly review an exam employing multiple perspectives and test conditions.

Imaging data are stored in a Digital Imaging and Communications in Medicine (DICOM) format and permit image post-processing which includes image annotation and manipulation such as highlighting a focal area of disease or 3D image reconstruction. Key anatomic landmarks or pathophysiologic features can be annotated and regions of interest can be highlighted to help orientate students to what is relevant and salient to lesson objectives. In addition, frame rates can be adjusted (e.g., hastened or slowed) to permit improved visualization and understanding of the disease mechanism being taught. Although stored in DICOM format, cine-loops can be exported to a number of common media formats. One format in particular, an animated Graphics Interchange Format (GIF), is potentially well adapted to presenting cine-loops. The cyclic nature of cardiac function dovetails nicely with infinite loop GIF capabilities. ²⁰ This feature allows the instructor to repeatedly present and thoroughly review all radiographic features and how they relate to the disorder at hand.

Before proceeding, it is imperative to state, without equivocation, that we are not proposing a preclinical curriculum in radiology. Student image interpretation is not the purpose of our proposal nor is a comprehensive explanation of imaging physics. Instead, the emphasis is on providing clear and concise case examples of CVD pathophysiology. Nevertheless, this endeavor would require close collaboration with radiology to ensure the basic educational goal is satisfactorily met. Case images must unambiguously demonstrate the principal manifestations of the disorder being taught. Cases should have minimal comorbidity to avoid distraction and student fixation on inappropriate material. This entails that all images are selected and edited by qualified radiologists. This would ensure that any case presented is relevant and of sufficient teaching quality. An additional requirement would also include defining relevant terminology that is specific to understanding the pathophysiology of the taught subject. This practice provides not only a level of quality assurance but also allows cases to be competently presented by non-radiologists such as pathology instructors.

Benefits to pathophysiology teaching

Pathophysiology is a fundamental important part of the basic science medical curriculum which provides a core understanding of the pathobiological basis of disease. ²¹ The subject bridges the gap between basic medical sciences and clinical training by describing the dysfunctional processes that occur in a disease state. ²² Pathophysiology, at its most basic tenant, is to acquaint medical students with the clinical manifestations of disease as a result of impaired biological function in a living system. ²³

Teaching concepts in pathophysiology is often a daunting task as it requires students to create a dynamic mental image of the dysfunctional kinetics and hemodynamics of CVD. Traditionally, these pathophysiologic concepts were demonstrated in animal-based laboratory sessions. However, animal use-related ethics, human applicability, and cost have made these traditional techniques anachronisms in modern scientific education.^{24 –26} Alternatives to animal-based instruction exist and include manikin-based simulation or computational simulation.^{27 –29} A full review of the available simulators is beyond the scope of this article. Nevertheless, a salient point bears mentioning. According to Okuda et al., ³⁰ evidence supports the use of simulation when teaching basic science has led to improved medical knowledge. To our knowledge, pathophysiology concepts taught in this fashion appear limited to clinical presentation (e.g., vital signs) and are not integrated with dynamic imaging to aid in explaining the pathophysiologic reasons for the patient’s clinical manifestations.

There is preliminary data to support using dynamic imaging as a teaching aid. Hammoudi et al. ³¹ used US imaging to instruct students on cardiac anatomy and physiology. Two-dimensional views were used to identify anatomical points and color Doppler US (i.e., echocardiography) was used to illustrate blood flow. Survey results indicated that a majority of students found cardiac US imaging improved their understanding of cardiac anatomy and physiology. Bell et al. ³² focused on teaching students the dynamic changes the left ventricle undergoes during cardiac cycles. Instruction was done through student-obtained parasternal long-axis cine-loops on standardized patients. Results, in regard to improved understanding and function visualization, were overwhelmingly positive. In addition, the ability to repeatedly review loops (i.e., backward and forward scrolling) was well received. Paganini and Rubini ³³ also used the US to demonstrate respiratory physiology which included cardiac kinetics. The authors argued the effectiveness of integrating real-time US into physiology instruction was based on the ability of the US to display the internal dynamics of a living system. They concluded that the utility of the US as a teaching aid should be further investigated. It is noteworthy that Jang et al. ³⁴ demonstrated that students in later clinical years generally believed that their study of dynamic radiologic images during the preclinical gross anatomy course was helpful for their clinical studies and clerkship rotations. Moreover, it was reported that student scores on anatomy examinations demonstrated meaningful improvements in performance after using dynamic images from CT and MRI.

The previously discussed articles provide strong evidence of the potential impact dynamic imaging can have on teaching the complex physiology of a dynamic organ. Nevertheless, these articles predominately focused on US imaging-based cardiac physiology of presumed healthy volunteers. Demonstration of CVD pathophysiology would, of course, require actual cases of specific diseases. Rather than relying on volunteers, a well-curated library of cases would mitigate a number of encumbering factors associated with real-time labs. Pre-selected scans can be standardized, including annotation and post-processing requirements, to present students with material directly relevant to the subject at an appropriate learning level. Preselected cine-loops would reduce costs associated with obtaining live scans, particularly where MRI is involved. This also applies to the high cost of mannikin simulators. ³⁵ In addition, the use of human data meets the 3R (Replacement, Reduction, and Refinement) principles in regard to animal usage. ³⁶ A final mention concerns the use of stress testing (e.g., pharmaceutical or exercise) to test for functional signs of ischemic heart disease primarily due to coronary artery disease.^37,38 Baseline images are obtained prior to induction of stress, which if positive, will result in wall motion abnormalities in both echocardiogram and CMR. It also presents an opportunity to demonstrate and teach via dynamic imaging, the sex-specific pathophysiologic consequences of CVD. This dovetails nicely with the increasing awareness of gender-specific manifestations of disease with dynamic pictorial means.^39,40 In addition, CMR can detect myocardial perfusion defects with the use of gadolinium contrast. While the student does not actually perform the intervention, the graphic display of interventional effects in a controlled environment is certainly in keeping with the spirit of putting theoretical knowledge into practice.

In summary, the use of cine-loop imaging is perfectly adapted to dynamically illustrate disease pathophysiology in a living body. Dynamic imaging students correlate the internal consequences of organ dysfunction with patient presentation thus improving their clinical acumen.

Benefits to radiology

Although we stated that our proposal should not serve as a preclinical radiology course, there are tangible benefits to the discipline. Practically since its inception, there has been a desire to incorporate radiology in preclinical medical education. ⁴¹ Radiographs have been used to augment instruction in subjects such as anatomy, histology, physiology, and pathology.^{42 –45} Integration of radiology in these basic science subjects has been largely positive. ⁴⁶ Success has been measured in terms of enhanced subject comprehension, improved material retention, and positive reception by students.^31,33,47 While the utility of radiographs in teaching basic sciences is undisputed, radiology itself remains a preclinical orphan, particularly in North American medical schools. ⁴²

While our proposal argues that images are prepared in such a way that non-radiologists can present the material, this does not invalidate the crucial role radiology must play in its development. To properly and competently present any radiographic-based educational material absolutely requires close collaboration with radiologists. At the minimum, this would ensure presented material is of sufficient quality and presented in a competent and coherent style.

Further benefits to radiology include an early introduction to the discipline and the important integrated role radiology plays in the multidisciplinary diagnosis and management of the disease. Other benefits of early integration of imaging into the preclinical basic sciences include demonstrating the technological capabilities of modern imaging techniques.

Our proposal does fall short of the stated aspirations by Gunderman et al. ⁴¹ regarding the need for a preclinical radiology course taught by radiologists. Nonetheless, our proposal requires the absolute, if indirect, cooperation of radiology. Conversely, this may address the problem of lost clinical time and revenue generation that may be incurred with teaching duties which was brought up in the aforementioned article. By having radiologists prepare the cases, non-radiologists can present the material competently and mitigate the need for radiologists to step away from clinical duties.

Conclusion

To our knowledge, our proposal appears to be original in regard to the use of specialized cine-loop technology to teach the dynamics of CVD pathophysiology. Dynamic imaging, including CMR, has been proposed and utilized in the past for teaching cardiac physiology.^{13,31 –33} Our proposal takes the principles one step further and applies them to teaching the functional impact of CV pathology on a living system.

Further investigation of this model of teaching would include generating evidence to support our proposal regarding comprehension of pathophysiologic concepts and application of this knowledge in practice. The task of appreciating signs and sequelae of pathognomonic dysfunction requires extensive use of the brain’s working memory. One potential solution to this problem is to present significant pathological content in a continuous visually dramatic mode. In the near future, cognitive load analysis may be performed to determine whether a difference in cognitive effort was experienced while utilizing dynamic imaging in a classroom setting. Usability studies might be conducted to evaluate the impact of dynamic imaging on exam performance and collect user experience metrics during a trial. Learning parameters of primary interest would include student comprehension, recall, and opinion on the teaching value of dynamic imaging of each modality. Certainly, our proposed approach could even be further explored utilizing the 3D reconstruction functionality of both discussed modalities. Other avenues worth investigating include integrating the aforementioned imaging modalities with other dynamic forms of clinical investigation such as electrocardiography or pulmonary function testing to further elucidate and teach concepts in pathophysiology. Ultimately, it would be necessary to confirm what impact dynamic imaging instruction has on the student’s clinical skills and competency.

Facta, non verba indeed; actions speak louder than words, and a picture in action speaks volumes.