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\begin{document}

\title{Perioperative Echocardiography Training: A Role for Ultra-high
Resolution Three-dimensional Printed Human Heart Models}



\author[1]{Paul Iaizzo}%
\author[1]{Susana Arango}%
\author[1]{Benjamin Gorbaty}%
\author[1]{John Brigham}%
\author[1]{Tjörvi E. Perry}%
\affil[1]{University of Minnesota Twin Cities Department of Surgery}%


\vspace{-1em}



  
  \date{May 18, 2024}


\begingroup
\let\center\flushleft
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\endgroup





\selectlanguage{english}
\begin{abstract}
Echocardiography is essential for diagnosing and assessing the severity
of perioperative structural and/or functional heart disease. Yet,
educational opportunities to better understand echocardiography-based
cardiac anatomy remain limited by the two-dimensional display, lack of
anatomic details, variability of heart models, and/or costs and global
availability of training. 3D printing using data from patient CT or MRI
datasets has been used for creating effective teaching materials,
although often it is limited by the resolutions. In this report, we
discuss the development of ultra-high resolution 3D printed human hearts
using \emph{ex vivo} microcomputed tomography (\selectlanguage{greek}μ\selectlanguage{english}CT) and describe its
utility for teaching both basic and advanced recommended views by the
American Society of Echocardiography.%
\end{abstract}%



\sloppy


Perioperative Echocardiography Training:

A Role for Ultra-high Resolution Three-dimensional Printed Human Heart
Models

Susana Arango, MD\textsuperscript{1,2}, Benjamin Gorbaty,
MD\textsuperscript{1}, John Brigham, MILS\textsuperscript{2},

Paul A. Iaizzo, PhD\textsuperscript{2}, Tj\selectlanguage{ngerman}örvi E. Perry,
MD\textsuperscript{1}

\textsuperscript{1} University of Minnesota, Division of Cardiothoracic
Anesthesia,

Department of Anesthesiology, Minneapolis, MN, USA

\textsuperscript{2}The Visible Heart® Laboratories, Department of
Surgery, Institute for Engineering in Medicine,

University of Minnesota, Minneapolis, MN, USA

\section*{Corresponding author:}

{\label{corresponding-author}}

Paul A. Iaizzo, PhD, FHRS

Department of Surgery, University of Minnesota,

B172 Mayo, MMC 195, Minneapolis, MN, 55455 USA

\textbf{Co-author emails:} Arango: arang023@umn.edu; Gorbaty:
bgorbaty@umn.edu; Brigham: cole0882@umn.edu; Iaizzo: iaizz001@umn.edu;
Perry: perry655@umn.edu

\textbf{Data availability:} Data are included in manuscript.

\textbf{Funding:} This work was supported by The Academic Investment
Program Grant from the University of Minnesota and MHealth (Minneapolis,
MN, USA).

\textbf{Conflict of interest:} The authors reported no conflicts of
interest.

\textbf{Ethics/Patient consent:} LifeSource, a regional organ
procurement agency, secured consent from donors and/or donor families,
then procured and donated human heart specimens deemed unsuitable for
transplantation to the Visible Heart®\textsuperscript{.} Laboratories
for research and education.



\textbf{Abstract}

Echocardiography is essential for diagnosing and assessing the severity
of perioperative structural and/or functional heart disease. Yet,
educational opportunities to better understand echocardiography-based
cardiac anatomy remain limited by the two-dimensional display, lack of
anatomic details, variability of heart models, and/or costs and global
availability of training. 3D printing using data from patient CT or MRI
datasets has been used for creating effective teaching materials,
although often it is limited by the resolutions. In this report, we
discuss the development of ultra-high resolution 3D printed human hearts
using \emph{ex vivo} microcomputed tomography (\selectlanguage{greek}μ\selectlanguage{english}CT) and describe its
utility for teaching both basic and advanced recommended views by the
American Society of Echocardiography.



\section*{Keywords}

{\label{keywords}}

3D printing; medical education; echocardiography; diagnostic ultrasound;
diagnostic imaging

\section*{Introduction}

{\label{introduction}}

Echocardiography is essential for diagnosing and assessing the severity
of perioperative structural and functional heart
disease.\textsuperscript{1-3} Educational opportunities to better
understand echocardiography-based cardiac anatomy and pathophysiology
during formal cardiology, anesthesiology, and surgical training programs
have traditionally been relegated to textbooks and/or online digital
resources. Yet, these often fail to convey a full appreciation of the
complex three-dimensional (3D) human cardiac anatomies. As a result,
3D-based simulators are becoming widely accepted. However, while they
seem accurate and adequate, these simulators often rely on handcrafted
models or CT datasets which lack the structural details and anatomic
variability routinely seen in clinical
practice.\textsuperscript{4}Today, gross cadaveric heart dissections are
becoming limited for financial, logistical, and social or cultural
barriers in some countries.

More recently, 3D printing of anatomic models, using data from scanned
images, has been leveraged for creating effective teaching
materials.\textsuperscript{5-7} At the same time, advances in imaging
technology allow for higher resolution datasets and translate directly
into higher resolution computational 3D modeling with unprecedented
anatomic details.\textsuperscript{8,9} 3D printed human
hearts\textsuperscript{6,10}, digital images, and virtual images are
being created using cardiac magnetic resonance imaging (cMRI), computed
tomography (CT), and echocardiographic imaging, \textsuperscript{6
10}yet these imaging technologies typically lack the resolutions to
accurately represent atrioventricular valvular and subvalvular anatomy
essential for advanced understanding of cardiac anatomy and surrounding
structures.\textsuperscript{5,11}

Finally, timely care delivery and productivity is often prioritized in
the cardiac operating room, leaving trainees with few and sporadic
opportunities for adequate perioperative echocardiography training.
Currently there are many other reasons why trainees across multiple
disciplines do not have optimized opportunities to learn the advanced
perioperative cardiac anatomy and pathology required for nuanced care
delivery during cardiac surgery, electrophysiologic ablation therapy,
and intracardiac catheter-based device delivery. Therefore, we developed
ultra-high resolution 3D printed human hearts using \emph{ex
vivo}microcomputed tomography (\selectlanguage{greek}μ\selectlanguage{english}CT) to teach basic and advanced American
Society of Echocardiography (ASE)-recommended cardiac ultrasound
views.\textsuperscript{1}

\textbf{Methods}

\section*{Data acquisition and 3D
modeling}

{\label{data-acquisition-and-3d-modeling}}

For several decades, the Visible Heart\selectlanguage{ngerman}® Laboratories at the University
of Minnesota have received gifted organs for research. To date, we have
perfusion-fixed more than 650 human hearts, utilizing this rich library
for generating education models for echocardiography training. Briefly,
following consent from donors and/or donor families, fresh human heart
specimens not suitable for orthotopic transplantation were procured by
LifeSource (Minneapolis, MN, USA) and donated to the Visible
Heart®\textsuperscript{.} Laboratories. In general, within hours of
explantation, the great vessels of these hearts were cannulated and then
perfusion-fixed with 10\% formalin for at least 24 hours to preserve an
approximation of the end-diastolic state.\textsuperscript{12} Prior to
imaging, each specimen was rinsed for a minimum of 12 hours to remove
any remaining formaldehyde.

Next, we performed \selectlanguage{greek}µ\selectlanguage{english}CT scans with 100\selectlanguage{greek}μ\selectlanguage{english}m resolution (X3000 CT, North Star
Imaging, Rogers, MN, USA) of the specimens, and imported anonymized
datasets into the post processing software Mimics\selectlanguage{ngerman}® Innovation Suite
(Materialise NV, Leuven, Belgium) to create high-resolution
computational 3D models using automatic, semi-automatic, and manual
segmentation methods.\textsuperscript{10} The cardiac walls, vessels,
and valves were typically segmented separately to create a mesh focused
on each specific structure(s). Next, the resulting 3D models were
exported as stereolithography (STL) files.

\section*{3D Printing}

{\label{d-printing}}

Models were edited accordingly and prepared for 3D printing using
3-Matic (Materialise NV). Typically, the surfaces of the model were
somewhat smoothed and any errors/gaps in the models were fixed.

\emph{Echocardiography Views Models}

We identified echocardiographic planes to represent different views as
recommended by ASE guidelines.\textsuperscript{1} For each computational
model, echocardiographic planes were digitally created and incorporated
into a heart model under the guidance and consensus of several
physicians trained and certified in advanced clinical echocardiography.
We labeled the models and created reciprocal holes (3.2 x 6.2 mm) to
accommodate magnets. Next, sets of magnets (3 x 6 mm) where embedded as
a means to hold corresponding pieces together.

We then printed the models to scale using a variety of 3D printers and
3D printing materials including an H350 Selective Absorption Fusion
powder bed printer with High Yield PA11 Nylon 11 (Stratasys, Eden
Prairie, MN, USA), a MakerBot Method X printer with white Tough
Polylactic Acid (PLA) (MakerBot, New York City, NY, USA), a uPrint with
Acrylonitrile Butadiene Styrene (ABS) (Stratasys), and an Ultimaker
3Extended with PolyLite\selectlanguage{english} PLA (Ultimaker B.V., Geldermalsen, The
Netherlands).

\emph{Isolated Valvular Structures}

We also printed the mitral and tricuspid valves utilizing a J750 Digital
Anatomy printer (Stratasys), using anatomical presets for moderately
stiff valve annulus material (blending VeroUltraWhite, TissueMatrix, and
Agilus30Clear) and 706B support material.



\section*{Results}

{\label{results}}

From the 650+ fixed specimens in our Human Heart Library, we chose to
image and generate models from a variety of hearts. These specimens were
selected primarily based on how well the cardiac anatomy was preserved
following explantation, as well as cardiac disease state. For our
initial educational purposes, we scanned, modeled, and printed models
from 4 different human hearts selected from our human heart library
(Table 1). The \emph{ex vivo} CT imaging of these specimens provided
high-resolution detail of the atrioventricular valves and corresponding
subvalvular structures (\emph{\textbf{Figs. 1,2}).} ASE-recommended
transesophageal echocardiography (TEE) views \emph{(\textbf{Fig. 3})}and
transthoracic echocardiography (TTE) Focus Assessed Transthoracic Echo
(FATE) views \emph{(\textbf{Fig. 4})} were selected for representation
by identifying and matching planes for each generated model
(Supplemental Video 1 ).

The cost of materials to print each heart model ranged between \$80-120
USD, the printing time spanned 14-80 hours per model, and the weights of
each model were between 250 and 400 g depending on the general
quality/durability of the selected material, the 3D printer, and the
size of the model. Note that once all models were optimized, the costs
and printing times could be reduced. Further, the average cost of each
3D printed valve was \$50 USD, and the time required for printing was 8
hours.

\textbf{Educational Uses}

These generated 3D printed cardiac models are readily available to
residents, cardiothoracic anesthesia (CTA) fellows, and attendings in
each cardiac operating room at the University of Minnesota Medical
Center. At our institution, these models are routinely used for teaching
residents and CTA fellows about basic and advanced echocardiographic
views, cardiopulmonary bypass cannulation strategies, and valvular
pathology and planned interventions (Figs. 5,6 ) in both normal and
pathological states (Fig. 7).

We also share the ready-to-print 3D models with the public through the
free-access Atlas of Human Cardiac Anatomy website
(http://www.vhlab.umn.edu/atlas/). We are committed to our mission to
provide world\selectlanguage{english}-class educational materials for anyone, anywhere.

\section*{Discussion}

{\label{discussion}}

We described a novel computational methodology using \selectlanguage{greek}μ\selectlanguage{english}CT to 3D print
ultra-high resolution human hearts in the form of ASE-recommended TEE
and TTE FATE views to facilitate advanced understanding of perioperative
echocardiography. We envision using these models to facilitate accurate,
high-resolution 3D visualization and tactile feedback to accelerate
memorizing absolute and relative cardiac anatomy. While formal studies
comparing traditional methods for teaching perioperative TEE with our 3D
printed human hearts are forthcoming, we have implemented this teaching
tool as an adjunct to be used in the operating and procedure rooms for
instructing anesthesia residents and cardiothoracic anesthesia fellows.

We consider that visualizing cardiac anatomy, both absolute and
relative, in various 3D perspectives can improve spatial recognition and
understanding while learning perioperative
echocardiography.\textsuperscript{13,14} Although published data are
sparse, Radzi and colleagues used CT imaging to generate 3D printed
hearts as means to teach cardiac anatomy.\textsuperscript{13} Limited by
their imaging technologies, this group reported difficulties while
segmenting the mitral and tricuspid valves. In a recent comparative
study including 153 medical students, Salewski and coworkers reported a
significant advantage in using 3D printed heart models when compared
with conventional educational resources, despite using CT
image-generated models from the Resuscitative TEE Project that lacked
atrioventricular valves.\textsuperscript{6} It should be noted that
Ochoa et al. reported no benefit in using low-resolution generic plastic
3D models sliced to represent echo views; this is contradictory to
results from other groups, and perhaps the result of the smaller group
size of only 20 medical students surveyed.\textsuperscript{15}

Building on this prior work, we used \selectlanguage{greek}μ\selectlanguage{english}CT technology to accurately
represent the valvular and subvalvular anatomies of the atrioventricular
valves. With our ability to represent cardiac anatomy and pathology in
ultra-high resolution 3D models, including the atrioventricular valves
and associated anatomy, we are confident that these educational tools
can significantly accelerate cardiac anatomic understanding in a safe
and predictable manner. Moreover, by generating multiple unique prints
of our ultra-high resolution heart models to represent each 2D plane of
the ASE-recommended TEE and FATE TTE views, we have effectively
transferred relatively low-resolution two-dimensional images from the
echocardiography machine into ultra-high resolution, low cost, durable,
and portable models that can be manipulated and studied, again and again
in a safe and predictable environment within or outside the operating
room. Notably our generated high-resolution cardiac models can be
printed using a variety of 3D printers employing a range of materials;
this should allow others to adjust materials, weights, and time of 3D
printing relative to the system available. By using these types of files
that are compatible with a range of 3D printing technologies, we plan to
make possible unrestricted and equitable access to our high-resolution
3D cardiac echo models.

We have identified various limitations in using our cardiac models to
teach anesthesia residents and cardiothoracic anesthesia fellows. Our
current models do not include extended portions of the great vessels.
Thus we have combined \emph{in vivo} cMRI or CT images with our \emph{ex
vivo} \selectlanguage{greek}μ\selectlanguage{english}CT images in an effort to add great vessel
anatomies.\textsuperscript{16} Furthermore, we have printed the
myocardium and valves with rigid materials that do not accurately
represent the dynamics of the cardiac anatomies. We are currently
experimenting with printing the various cardiac structures including the
myocardium, valve annuli, leaflets, and chordae tendinea in more pliable
materials that allow learners to experience valve and leaflet positions.
Finally, we need to generate high-resolution models with valves
representing all phases of the cardiac cycle, work that is ongoing by
our team.

\section*{Conclusions}

{\label{conclusions}}

Representing the human heart by ultra-high resolution 3D models, printed
to display ASE-recommended echocardiographic views, is now feasible by
using \selectlanguage{greek}μ\selectlanguage{english}CT imaging of perfusion-fixed human heart specimens. In so doing,
we have generated a library of printed hearts as a unique educational
tool designed to accelerate, rapidly and safely, the understanding of
absolute and relative human cardiac anatomy and pathology, especially
related to gaining advanced appreciation of clinically employed
perioperative echocardiography.

\section*{Acknowledgments}

{\label{acknowledgments}}

The Visible Heart\selectlanguage{ngerman}\textsuperscript{®} Laboratories are grateful to the
patients and their families who have donated human heart specimens for
research, and to LifeSource for assistance in the recovery and transport
of these organs. We thank Stratasys for their collaboration relative to
3D prints and material donations.

\section*{References}

{\label{references}}

\begin{enumerate}
\tightlist
\item
  Hahn, R. T., Abraham, T., Adams, M. S., Bruce, C. J., Glas, K. E.,
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\item
  Vahanian, A., Beyersdorf, F., Praz, F., Milojevic, M., Baldus, S.,
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\item
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\item
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\end{enumerate}

\textbf{Figure Legends}

\textbf{Figure 1} . 3D printed models of HH 229. Slice on the left
represents a transthoracic echocardiography (TTE) parasternal long-axis
view, and that on the right represents the transesophageal
echocardiography (TEE) mid-esophageal and transgastric long-axis view.
Ao=aorta; LA=left atrium; LV=left ventricle; LVOT=left ventricular
outflow tract; RV=right ventricle.

\textbf{Figure 2.} 3D printed model of the tricuspid valve of HH 223.
(A) Model printed in clear material as viewed from the atrium with
leaflets labeled and the moderator band marked with red arrow. (B) Model
printed using multiple colors and materials and rotated to appreciate
the subvalvular apparatus. Yellow, tricuspid annulus; transparent,
mitral leaflets; blue, chordae tendinea; pink, papillary muscles.

\textbf{Figure 3.} High-resolution fusion powder 3D printed heart models
representing the transesophageal echocardiography (TEE) American Society
of Echocardiography (ASE)-recommended views. Each row represents two
corresponding planes on each model that have been labeled accordingly.
LAX=long-axis; RV=right ventricle; SAX=short-axis; TG=transgastric.

\textbf{Figure 4.} High-resolution fusion powder 3D printed heart model
representing the Focus Assessed Transthoracic Echo (FATE ) views (A)
composed of 8 pieces representing (B) the parasternal long-axis view,
(C) parasternal short-axis view, and (D) apical four-chamber and/or
subcostal view.

\textbf{Figure 5.} 3D printed models being utilized by trainees within
the operating room during a transesophageal echocardiography (TEE)
educational opportunity. (A) transgastric short-axis (TG SAX) view, (B)
midesophageal long-axis (ME LAX) view, and (C) four-chamber view.

\textbf{Figure 6.} 3D printed model of mitral valve being utilized by
trainees within the operating room during a transesophageal
echocardiography (TEE) educational opportunity.

\textbf{Figure 7.} 3D printed models of HH 281. Slice represents a
transesophageal echocardiography (TEE) mid-esophageal long-axis view of
a heart with severe hypertrophic cardiomyopathy. The left atrium was
removed during explantation. (A) Mitral valve, (B) left ventricle, (C)
aortic valve, (D) right ventricle, (E) hypertrophic interventricular.

\textbf{Supplemental Video 1.} High-resolution 3D printed human heart
model sliced in four-chamber and two-chamber views. The reciprocal
pieces are held together by magnets.

\textbf{Table 1.} Human heart demographics and medical history\selectlanguage{english}
\begin{longtable}[]{@{}llll@{}}
\toprule
\begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
Human Heart Specimen\strut
\end{minipage} & \begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
Patient Age (yr)\strut
\end{minipage} & \begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
Patient Gender\strut
\end{minipage} & \begin{minipage}[b]{0.24\columnwidth}\raggedright\strut
Medical History\strut
\end{minipage}\tabularnewline
\midrule
\endhead
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
HH103\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
68\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
M\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Arterial hypertension, diabetes mellitus, atrial fibrillation, atrial
septal defect\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
HH223\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
56\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
M\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Coronary artery disease, obstructive sleep apnea\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
HH229\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
44\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
F\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Arterial hypertension, heart failure\strut
\end{minipage}\tabularnewline
\begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
HH281\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
14\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
F\strut
\end{minipage} & \begin{minipage}[t]{0.22\columnwidth}\raggedright\strut
Hypertrophic cardiomyopathy\strut
\end{minipage}\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{english}
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