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Aortic Hemodynamics of Spiral-Flow-Generated Mechanical Assistance
Journal Pre-proof Aortic Hemodynamics of Spiral-Flow-Generated Mechanical Assistance Pablo Huang Zhang, PhD, Colin Tkatch, MD, Dmitri Vainchtein, PhD, J. Yasha Kresh, PhD PII:
S0003-4975(19)31414-6
DOI:
https://doi.org/10.1016/j.athoracsur.2019.08.028
Reference:
ATS 33050
To appear in:
The Annals of Thoracic Surgery
Received Date: 18 January 2019 Revised Date:
6 June 2019
Accepted Date: 8 August 2019
Please cite this article as: Zhang PH, Tkatch C, Vainchtein D, Kresh JY, Aortic Hemodynamics of Spiral-Flow-Generated Mechanical Assistance, The Annals of Thoracic Surgery (2019), doi: https:// doi.org/10.1016/j.athoracsur.2019.08.028. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 by The Society of Thoracic Surgeons
Aortic Hemodynamics of Spiral-Flow-Generated Mechanical Assistance Running Head: Spiral Flow Dynamics: MCS to the Aorta
Pablo Huang Zhang, PhD1, Colin Tkatch, MD2, Dmitri Vainchtein, PhD3, J. Yasha Kresh, PhD1,2
1
Department of Cardiothoracic Surgery, Drexel University College of Medicine;
2
Department of Medicine-HUP, IME-University of Pennsylvania
3
C. & J. Nyheim Plasma Institute, Drexel University
Philadelphia, PA, USA
Key Words: Aortic Hemodynamics, Spiral Flow, Computational Fluid Dynamics, Mechanical Circulatory Support, Outflow Graft
Word Count, Abstract: 243 Total: 4,483
Corresponding Author: J. Yasha Kresh, PhD, FACC FAHA Department of Cardiothoracic Surgery Hahnemann University Hospital Drexel University College of Medicine 245 N. 15th Street, Room-6320, Mail Stop#111 Philadelphia, PA 19102 [email protected]
1
Abstract Background: Mechanical circulatory support (MCS) devices are being increasingly used as destination therapy in end-stage heart failure patients. Although current devices have significantly improved survival rates, the resulting hemodynamics remains non-physiological. Spiral forms of blood flow are known to exist in the large arteries (e.g., aorta) and serve as a biomimetic-motivation for generating these physiologically-adapted flow regimes. This research aimed to study the potential benefits of generating spiral flow at the MCS outflow graft and the resultant flow-fields in the aorta, including recirculation zones and endothelial wall shear stress (WSS) areas. Methods: A 3D-model of an outflow graft virtually anastomosed end-to-side to an imagederived aortic arch was used in computational fluid dynamic simulations. To study the impact of both spiral flow modulation (clockwise/counter-clockwise helical-flow content) and the outflow graft anastomosis angle (inferiorly/superiorly-directed, anteriorly/posteriorly-directed), flow velocities were measured, low/high-WSS were computed, and fluid streamlines were visualized. Results: Increased helical-flow content reduced regions of low-velocity (<5cm/s), minimized areas exhibiting low-WSS (<3dyn/cm2), and concomitantly increased areas of high-WSS (>80dyn/cm2). The outflow graft anastomosis angle was a key determinant of aortic root washout and fluid-jet wall impingement. Despite counter-clockwise spiral flow predominance in diminishing the size of recirculation/stasis zones compared to straight/clockwise flow, exceptions to this were noted with the superiorly-directed and posteriorly-directed graft placements. Conclusions: Spiral flow-forms better tailored to the underlying three-dimensional aortic curvature and graft angle positioning is expected to help attenuate atherogenesis, preventing vascular remodeling and minimizing plaque formation/erosion in mechanically assisted circulation.
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Heart disease is the leading cause of death in the United States, annually contributing to about a quarter of all deaths nationwide (1). Technological advancements of continuous-flow mechanical circulatory support (MCS) devices for patients with heart failure have increasingly led to their use not only as a bridge-to-transplant, but as a destination therapy (2). While current MCS devices can maintain blood circulation, complications such as bleeding, thromboembolic events, infection, and inflow suction-induced arrhythmias limit optimal outcomes (3, 4). Using biologically-inspired spiral forms of flow, this work explores how the manipulation of MCS outflow characteristics can ameliorate device mediated vascular complications.
Spiral blood flow, consisting of combined axial and circumferential flow fields, has been identified throughout the cardiovascular system and postulated to offer several hemodynamic benefits, including the normalization of wall shear stress (WSS) gradients (5-8). WSS is a fluidvelocity-induced tangential force that plays an important role in endothelial cell mechanosignaling. It is well understood that prolonged exposure to low-WSS induces flow-mediated endothelial cell mis-patterning, leading to increased vascular wall permeability and subsequent atherothrombotic risk/development (9). Conversely, excessively high-WSS can lead to vascular wall fatigue and platelet activation.
Several studies have reported on the benefits of producing/propagating spiral flow in the arterial system. For example, Houston et al. demonstrated that patients with severe renal artery stenosis and decreased native spiral flow prevalence exhibited accelerated progression of renal impairment (10). Chen et al. determined that endovascular stent designs with spiral flow generation promoted the reduction of flow disturbance regions and an increase in average endothelial WSS (11). Using numerical simulations, Deng et al. reported that generation and propagation of spiral flow in the aortic arch reduced luminal surface low-density lipoprotein concentration, limiting the development of atherosclerosis (12). Spiral flow has also been shown
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to reduce platelet adhesion to collagen-coated surfaces in sudden expansion conduit models, without impacting platelet activation potential (13). Finally, spiral flow has been shown to limit energy dissipation and turbulence while reducing areas of recirculation/stasis in stenotic vascular models (14). It is important to also recognize pathological forms of spiral flow; they usually have very short helical wavelengths and can manifest in instances of bicuspid aortic valve (15).
Positioning and angle of the MCS device outflow graft have consequential effects on aortic arch hemodynamics (16, 17). May-Newman et al. used an idealized aorta model and computational fluid dynamic (CFD) approach to show that the outflow graft positioning significantly affected flow disturbance and washout in the aortic arch, especially in patients with diminished native aortic root flow (18). Caruso et al. studied the vertical positioning of the outflow graft and emphasized the importance of balancing flow organization in the aortic arch with disease-prone recirculation regions in the ascending aorta (19). Several studies have shown that a shallow anastomotic angle with respect to the ascending aorta reduced the development of pathologic secondary flow and minimized embolization potential to the cerebral vessels (17, 20, 21).
While several studies have looked at the outflow graft positioning and angle, few have evaluated the aortic hemodynamics of incorporating spiral flow mechanics to the MCS outflow. The presented research aimed to study the biomechanical and hemodynamic impact of spiral forms of flow at the MCS outflow graft – aorta interface. It is well known that the fluid jetting caused by MCS devices drastically alters the aortic flow patterns, introducing pathophysiological flow regimes affecting the vascular response. The effects of the intensity of spiral flow modulation and the insertion angle of the outflow graft were evaluated in terms of previously established benefits: normalization of WSS gradients, diminishing high-velocity jet-flow on the
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vascular wall (impingement), and reduction of regions of low flow. This work is not only expected to inform future MCS device designs by elucidating the beneficial role of spiral flow as an organizational force, but also to provide greater understanding in surgical practice for minimizing progression of flow-induced vascular disease and related adverse clinical outcomes (e.g., intimal hyperplasia, atheroma erosion).
Material and Methods Three computational fluid dynamic (CFD) sub-studies were conducted using a 3Dimage-derived patient aortic arch model, obtained from an online repository (Stratasys, Cambridge, MA). This model was modified using SolidWorks (Dassault Systemes, VelizyVillacoublay, France) to include a laterally-positioned outflow graft (1.6cm diameter) virtually anastomosed end-to-side 2cm below the brachiocephalic trunk (Figure 1). The first sub-study evaluated the effects of spiral flow modulation, introduced at the laterally-positioned outflow graft, on aortic arch hemodynamics. To define the spiral flow intensity, the rotation (revolutions per minute, RPM) and direction (+/- denoting clockwise/counter-clockwise, respectively) of the graft outflow was set to 0, ±70, ±160, ±318, and ±500 RPM. Using straight flow as control and ±160RPM for the spiral flow conditions, the second and third sub-studies evaluated the combined effects of the graft insertion angle and spiral flow content. With respect to the laterally-positioned graft anastomosis (serving as the zero-reference position), the graft was directed inferiorly/superiorly by 20° ( second sub-study), and directed anteriorly/posteriorly by 20° ( third sub-study) (Figure 1).
Computational Fluid Dynamic (CFD) Simulations The open source software OpenFOAM (ESI, Bracknell, UK) was used for the 3D mesh generation and fluid dynamic simulations. The mesh for the aorta model consisted of 1.5 million hexahedral cells. A mesh refinement study was completed using the outflow graft fluid jet
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velocity and the impact WSS as convergence parameters to ensure that the computed results were representative of the flow dynamics (given the geometry and initial conditions) and not due to insufficient analytical-grid resolution of the fluid domain. The working fluid (blood) was modeled as an incompressible Newtonian fluid with a density of 1.06g/cm3 and a viscosity of 4.1cP. A transient solver incorporating turbulence modeling was used to solve the equations (Navier-Stokes) governing fluid dynamics.
No-slip boundary conditions were implemented at all vessel walls, which were assumed to be rigid. Continuous flow 5L/min was generated at the graft simulating MCS outflow, and 1L/min at the aortic root inlet simulating the impaired cardiac output. Spiral flow with variable helical content was implemented at the graft inlet using a rate of rotation (RPM) condition. The 70RPM was chosen to mimic the average human heart rate of 70 beats per minute; 318RPM was used to generate a single helix with a wavelength equivalent to the distance between the modeled graft inlet and the inner curvature of the ascending aorta; 160RPM generated a wavelength twice that of 318RPM; 500RPM generated a wavelength equal to the graft length used in the model (Figure 1). Straight (0 RPM) flow-condition was used at the aortic root inlet boundary and also served as the control-case for the MCS outflow graft.
Analysis and Visualization Post-processing/analysis was conducted using an open-source visualization software (ParaView, Kitware, NY). To evaluate flow disturbance and high-velocity fluid jetting, velocitycolored streamlines and areas of wall shear stress (WSS) were visualized. To quantify and assess the size of atheroprone regions and the impact of high fluid velocity jets, volumes of lowvelocity (<5cm/s), areas of low-WSS (<3dyn/cm2), and areas of high-WSS (>80dyn/cm2) were extracted using threshold analysis methods. The low-WSS cutoff value is associated with
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atherothrombotic risk due to flow-mediated endothelial dysfunction, while the high-WSS value is associated with shear-induced platelet activation.
Results First Sub-Study: Laterally-Positioned Outflow Graft Spiral Flow Modulation The velocity-colored streamlines resulting from the spiral flow modulation at the inlet of the end-to-side, laterally-placed outflow graft are shown in Figure 2. Areas of low-WSS were superimposed on the streamlines to identify regions vulnerable to endothelial dysfunction. Despite the induced straight flow at the graft, the control case exhibited swirling features at the descending aorta, attributed primarily to the additive effects of the aortic arch curvature and three-dimensional torsional geometry of the ascending and descending segments (out-of-plane geometry). The ‘braiding/weaving’ of the streamlines was significantly different for the straight, clockwise, and counter-clockwise flow conditions. As the helical-flow content increased, the high-velocity jetting (red streamlines, Figure 2) at the arch diminished, affecting the size of the recirculation pockets at the descending segment of the aorta. Concurrently, the areas of lowWSS at the aortic root decreased in size with increasing helical-flow content.
Quantitatively, as the helical-flow content increased, the volume of low-velocity in the fluid domain diminished (Figure 3). With the exception of the 500RPM case, counter-clockwise graft flow predominantly minimized regions of low-velocity. With the 500RPM case, clockwise flow decreased the volume of low-velocity by 2.1-fold and counter-clockwise by 1.4-fold, when compared to straight flow.
Spiral flow markedly altered the WSS response, principally decreasing the size of lowWSS area with increasing helical-flow content (Figure 3). At the highest helical-flow content,
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clockwise flow exhibited a 1.5-fold decrease and counter-clockwise flow yielded a 1.2-fold reduction in low-WSS area when compared to straight flow. Despite the reduction of low-WSS areas, higher helical-flow content (e.g., 500RPM) demonstrated increased size of high-WSS areas at the ascending aorta. The highest helical-flow content had on average a 1.3-fold size increase in high-WSS area (actual values exceeding 150dyn/cm2) when compared to straight flow. The 160RPM counter-clockwise flow regime exhibited the smallest area of high-WSS, while also reducing the size of regions with low-velocity and areas of low-WSS. This spiral flow regime was used for two subsequent outflow graft insertion angle variation sub-studies.
Second Sub-Study: Inferiorly/Superiorly-Directed Outflow Graft To study the combined effects of MCS spiral outflow and graft angle variation on aortic hemodynamics, the graft anastomosis angle was directed inferiorly and superiorly (by 20°) with respect to the lateral positioning. The angle of the graft affected the distribution of the highvelocities (colored in red) at the arch and the low-WSS areas at the aortic root (Figure 4). The inferiorly-directed graft had the best clearance of the areas of low-WSS at the root, but caused the high-velocity jets to concentrate on the inner curvature of the ascending aorta creating an impingement force on the wall. The superiorly-directed graft focused high velocities towards the distal wall of the descending aorta, but resulted in the largest areas of low-WSS at the aortic root.
The inferiorly-directed graft anastomosis demonstrated smaller volumes of low-velocity and diminished areas of low-WSS. Straight flow regime for the inferiorly-directed graft had on average a 1.6-fold reduction in low-velocity volume compared to other graft angles (Figure 5). Counter-clockwise graft flow improved predominantly the clearance of low-velocity and lowWSS, and decreased areas of high-WSS created by the fluid-jet impingement, compared to
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straight and clockwise flows. For the inferiorly-directed and lateral grafts, there was a 1.2-fold decrease in low-velocity for counter-clockwise flow compared to straight flow; superiorlydirected graft positioning had a marginal reduction in low-velocity with counter-clockwise flow, compared to straight flow. Although the inferiorly-directed graft positioning was better in diminishing low-WSS areas, it increased the areas of high-WSS, specifically at the fluid jet impact site located contralaterally to the graft outflow (i.e., inner curvature of the arch). However, when compared to straight flow, inducing a clockwise flow in the inferiorly-directed outflow graft yielded a 1.1-fold decrease in size of high-WSS areas, while counter-clockwise flow yielded a 1.4-fold decrease.
Third Sub-Study: Anteriorly/Posteriorly-Directed Outflow Graft The anastomosis angle of the MCS outflow was additionally varied in the transverse plane, directing the graft anteriorly and posteriorly by 20° with respect to the lateral-positioning. In the posteriorly-directed graft, the induced spiral flow increased the size of low-velocity regions and areas of low-WSS (Figure 6). In the anteriorly-directed anastomosis there was no significant improvement in these values with imposed spiral flow. However, high-WSS was significantly affected by varying the transverse angle and adding spiral flow. The anteriorlydirected graft demonstrated a substantially smaller area of high-WSS, where counter-clockwise flow produced a 13.2-fold reduction compared to straight flow. For the posteriorly-directed graft, counter-clockwise flow yielded a 1.15-fold increase in high-WSS area size compared to straight flow. This distinct difference when using counter-clockwise flow can be attributed to the resultant anastomosis-angle-induced fluid jet vascular wall impingement.
Comment The goal of this study was to create an in-silico platform to formulate an integrative understanding of spiral blood flow generated at the MCS outflow graft and the resultant aortic
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hemodynamics. The prevailing three-dimensional curvature of the aorta imparts a natural spiral motion on blood flow which is unique for each patient. These aortic hemodynamic signatures are significantly altered by current MCS devices, which not only extinguish the native spiral flow patterns but also introduce disruptive fluid jets, causing recirculation zones and pathogenic regions of low-WSS, increasing the risk of vascular disease progression and complications (e.g., intimal hyperplasia, atheroma disruption/erosion). The hemodynamic outcomes of introducing spiral flow through an outflow graft, virtually anastomosed end-to-side to the ascending aortic arch of a patient-specific aorta model, were studied in detail.
The first sub-study demonstrated that by increasing the helical-flow content, the high velocities at the arch were diminished and the size of flow recirculation/stasis regions were reduced. The blood transport benefits of spiral flow were similarly observed by others (22, 23). Despite the improvement in areas of low-WSS, increasing helical-flow content (i.e. 500RPM) also increased the areas of WSS in excess of 80dyn/cm2, with overall highest measured peak WSS ~150dyn/cm2. This sub-study provided an important insight on spiral flow generation, establishing that a defined spiral structure (set helical intensity/direction) is not generic, requiring that the 3D vascular geometry of the individual patient should be considered.
In the second sub-study, the inferiorly-directed graft positioning demonstrated the smallest regions of low-velocity and reduced areas of low-WSS, due to the better-aimed washout of the aortic root. However, this configuration also increased the impact area WSS>80dyn/cm2 at the ascending aorta, which was moderated by the imposed spiral flow regimes (i.e., counter-clockwise). While counter-clockwise spiral flow improved overall washout parameters for the inferiorly-directed graft, the superiorly-directed graft fared marginally better with clockwise flow. The difference was largely due to the arch configuration itself; flow from the graft in the superiorly-directed position did not need to navigate the aortic curvature, aiming
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directly towards the descending aorta. Accordingly, the impact WSS areas were the smallest for the superiorly-directed graft.
The third sub-study emphasized the impact of transverse graft positioning on high-WSS areas. As illustrated in Figure 6, the transverse anastomosis placement significantly alters the expected flow trajectory, and consequential mechanical impingement on the wall. The anteriorly-directed graft had a considerably diminished wall impact (impingement) than the laterally-placed graft. The marked decrease in high-WSS in response to the counter-clockwise flow in the anteriorly-directed graft is a reflection of the inherent helical continuity of the fluid structure. This is a striking example of ‘form follows function’, where the modeled threedimensional aortic arch geometry naturally induced a counter-clockwise spiral flow-direction. Clockwise flow in the anteriorly-directed graft increased the wall impact, necessitated by the rotational switch-back (from clockwise to counter-clockwise) dictated by the aortic 3D-curvature. Conversely, the immediacy of the flow impingement on the posterior wall in the posteriorlydirected graft generated increased areas of high-WSS. Given the posterior location of the fluid impact, counter-clockwise graft flow caused the fluid to be forced into the wall, increasing the high-WSS. In this specific case, increasing the helical-flow intensity (higher RPM) in the clockwise direction may help circumnavigate the wall and thus minimize the fluid impact-force.
In evaluating the resultant complex aortic flow dynamics, spiral flow generation was shown to be instrumental in addressing problem regions due to outflow graft fluid jetting. The study provides several translational considerations pertinent to MCS surgical implant approaches. Orienting the MCS outflow graft to the downstream flow is preferable for minimizing areas of high-WSS (associated with vessel wall fatigue/weakening, erosion of pre-existing atheroma and subsequent embolic complication). With limited surgical window and accessibility, the graft placement should be directed to avoid nearby fluid jet impingement on the vascular
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wall. Spiral flow is expected to have broad utility: low helical-flow content can be used to navigate downstream vessel tortuosity in cases where the anastomosis positioning is unrestricted, while high helical-flow content can be used when access is limited and collision of the fluid jet with the vessel wall is unavoidable. Despite the benefits of spiral flow, the jet impact location (anterior/posterior or proximal/distal to the arch) and the preferred fluid-directing rotation of the native aorta should be carefully considered to avoid ‘switch-back’ in spiral directionality, which may contribute to the formation of disturbed flow. Spiral flow must be optimized and informed by the native geometry and flow/anastomosis conditions to prevent detrimental flow-form and vascular-structure mismatching.
There are a number of limitations to numerical modeling in general that need to be acknowledged. In particular, the aortic walls were modeled as rigid boundaries to simplify the chosen computational approach. Although these studies focused on continuous-flow with added spirality, it is important to recognize that in mechanically supported circulation the composite aortic flow preserves some pulsatility. Considering that spiral flow was shown to reduce highvelocity jetting, its role in ameliorating aortic dysfunction (e.g., insufficiency) shows promise and requires further investigation. Importantly, this study was confined to a single aorta model template, and although it did not address the full range of anatomical variations or exhaustively test all the degrees of freedom of the graft anastomosis positions, it created a working framework for testing explicit angles and conditions pertaining to individual surgical cases.
In conclusion, using an in-silico approach, a framework for understanding spiral flow and its associated benefits in assisted circulation was implemented in a patient-derived model of the aortic arch with a virtually anastomosed MCS-pump outflow graft. Specifically, the impact of spiral modulation of the graft outflow and the effect of the graft angle positioning in relation to the ascending aorta were studied. The results demonstrated that increased spiral flow reduced
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regions of low-velocity and areas of low-WSS, important hemodynamic determinants of vascular endothelial dysfunction. When optimized, matching of helical-flow content to the patient-specific vascular anatomy and flow conditions (rotational direction, helical pitch), spiral flow can be used to minimize endothelial-disruption by fluid jetting and improve washout of recirculation/stasis problem zones. Future MCS device designs, incorporating spiral-flow generating features may prove to be a desirable solution improving the hemodynamics of the aorta – outflow graft coupling. Several implantable medical devices (e.g., endovascular grafts, valves, cardiopulmonary bypass cannula) also stand to benefit from spiral flow-induced reduction of fluid flow disturbances and related mechanobiological molecular signaling responses, improving patient-individualized therapy.
Acknowledgement: Aorta model adapted/modified from https://grabcad.com/library/humananatomic-aorta-w-out-extension-1. Computational studies made possible by Proteus, Drexel University’s high-performance computer cluster. Simulation post-processing assistance by Robert Newman. Dmitri Vainchtein supported in part by the National Science Foundation: Award No. CMMI-1740777(D.L.V.).
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References 1.
Heron M. Deaths: Leading causes for 2015. Natl Vital Stat Rep 2017;66(5):1-76.
2.
Pinney SP, Anyanwu AC, Lala A, Teuteberg JJ, Uriel N, Mehra MR. Left ventricular
assist devices for lifelong support. Journal of the American College of Cardiology 2017;69(23):2845-2861. 3.
Slaughter MS, Pagani FD, Rogers JG et al. Clinical management of continuous-flow left
ventricular assist devices in advanced heart failure. The Journal of Heart and Lung Transplantation 2010;29(4, Supplement):S1-S39. 4.
Zhang PH, Kresh JY. Circulatory mechanotherapeutics: Moving with the force. Curr
Cardiol Rep 2018;20(10):94. 5.
Stonebridge PA, Hoskins PR, Allan PL, Belch JF. Spiral laminar flow in vivo. Clin Sci
(Lond) 1996;91(1):17-21. 6.
Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB. Helical and retrograde
secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 1993;88(5 Pt 1):2235-2247. 7.
Frazin LJ, Lanza G, Vonesh M et al. Functional chiral asymmetry in descending thoracic
aorta. Circulation 1990;82(6):1985-1994. 8.
Tanaka M, Sakamoto T, Sugawara S et al. Spiral systolic blood flow in the ascending
aorta and aortic arch analyzed by echo-dynamography. Journal of Cardiology 2010;56(1):97110. 9.
Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev
1995;75(3):519-560.
14
10.
Houston JG, Gandy SJ, Milne W, Dick JB, Belch JJ, Stonebridge PA. Spiral laminar flow
in the abdominal aorta: A predictor of renal impairment deterioration in patients with renal artery stenosis? Nephrol Dial Transplant 2004;19(7):1786-1791. 11.
Chen Z, Fan Y, Deng X, Xu Z. Swirling flow can suppress flow disturbances in
endovascular stents: A numerical study. ASAIO journal 2009;55(6):543-549. 12.
Liu X, Pu F, Fan Y, Deng X, Li D, Li S. A numerical study on the flow of blood and the
transport of ldl in the human aorta: The physiological significance of the helical flow in the aortic arch. American Journal of Physiology-Heart and Circulatory Physiology 2009;297(1):H163H170. 13.
Zhan F, Fan Y, Deng X, Xu Z. The beneficial effect of swirling flow on platelet adhesion
to the surface of a sudden tubular expansion tube: Its potential application in end-to-end arterial anastomosis. ASAIO journal 2010;56(3):172-179. 14.
Ha H, Lee SJ. Effect of swirling inlet condition on the flow field in a stenosed arterial
vessel model. Med Eng Phys 2014;36(1):119-128. 15.
Hope MD, Hope TA, Meadows AK et al. Bicuspid aortic valve: Four-dimensional mr
evaluation of ascending aortic systolic flow patterns. Radiology 2010;255(1):53-61. 16.
Litwak KN, Koenig SC, Tsukui H, Kihara Si, Wu Z, Pantalos GM. Effects of left
ventricular assist device support and outflow graft location upon aortic blood flow. ASAIO journal 2004;50(5):432-437. 17.
Chiu WC, Alemu Y, McLarty AJ, Einav S, Slepian MJ, Bluestein D. Ventricular assist
device implantation configurations impact overall mechanical circulatory support system thrombogenic potential. ASAIO journal 2017;63(3):285-292.
15
18.
May-Newman K, Hillen B, Dembitsky W. Effect of left ventricular assist device outflow
conduit anastomosis location on flow patterns in the native aorta. ASAIO journal 2006;52(2):132-139. 19.
Caruso MV, Gramigna V, Rossi M, Serraino GF, Renzulli A, Fragomeni G. A
computational fluid dynamics comparison between different outflow graft anastomosis locations of left ventricular assist device (lvad) in a patient-specific aortic model. International Journal for Numerical Methods in Biomedical Engineering 2015;31(2):e02700. 20.
Argueta-Morales R, Tran R, Ceballos A et al. Mathematical modeling of patient-specific
ventricular assist device implantation to reduce particulate embolization rate to cerebral vessels. Journal of biomechanical engineering 2014;136(7). 21.
Aliseda A, Chivukula VK, McGah P et al. Lvad outflow graft angle and thrombosis risk.
ASAIO journal 2017;63(1):14-23. 22.
Zhang Q, Gao B, Chang Y. Helical flow component of left ventricular assist devices
(lvads) outflow improves aortic hemodynamic states. Medical Science Monitor : International Medical Journal of Experimental and Clinical Research 2018;24:869-879. 23.
Morbiducci U, Gallo D, Cristofanelli S et al. A rational approach to defining principal axes
of multidirectional wall shear stress in realistic vascular geometries, with application to the study of the influence of helical flow on wall shear stress directionality in aorta. J Biomech 2015;48(6):899-906.
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Figure Legends
Figure 1: Model of the patient-specific aorta (right). The outflow graft was virtually anastomosed end-to-side to the ascending aorta in the lateral position. The first sub-study varied the helicalflow content of the outflow graft represented in terms of RPM (left-top, scaled illustration of the theoretical helical wavelength beginning at the graft inlet boundary). The second sub-study varied the anastomosed graft direction inferiorly/superiorly by 20° (left-middle), while the third sub-study directed the graft 20° anteriorly/posteriorly (lef t-bottom). RPM=revolutions/minute.
Figure 2: Velocity-colored streamlines resulting from the spiral flow modulation (clockwise, counter-clockwise) at the inlet of the laterally-placed outflow graft. Regions of WSS<3dyn/cm2 are superimposed to identify atherothrombotic-susceptible areas. Modulation of helical-flow content demonstrates altered fluid jet at the arch and the locality/size of the low-WSS regions. WSS=wall shear stress.
Figure 3: Compared to straight flow, increasing the helical-flow content decreases the volume of low-velocity regions (top). Except for the 500RPM condition, counter-clockwise flow performs better than clockwise flow. Despite smaller areas of low-WSS (bottom left), higher helical-flow content increases the areas of high-WSS (bottom right) at the aortic arch. RPM=revolutions/minute; WSS=wall shear stress.
Figure 4: Velocity-colored streamlines and superimposed WSS<3dyn/cm2 areas resulting from the inferiorly/superiorly-directed graft flow. High velocities (red streamlines) are spatially altered depending on the graft angle: the inferiorly-directed graft causes the fluid jet to impinge on the ascending arch, while the superiorly-directed graft diverts high velocities downstream. The
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inferiorly-directed graft exhibits better aortic root washout, compared to the superiorly-directed graft. RPM=revolutions/minute; WSS=wall shear stress.
Figure 5: The inferiorly-directed graft results in an overall smaller volume of low-velocity (top) and smaller areas of low-WSS (bottom left), but it creates more fluid jetting onto the wall as reflected by the high-WSS areas (bottom right). With the exception of the superiorly-directed graft position, the regions of low-velocity and areas of low-WSS are notably reduced by counterclockwise flow. For high-WSS (>80dyn/cm2), counter-clockwise flow significantly reduces the size of impacted regions. WSS=wall shear stress.
Figure 6: Shown in the left-most column is the top view of the graft flow-trajectory with respect to the transverse anastomosis angle. Adding spiral flow in the anteriorly-directed graft impacts minimally the regions of low-velocity (top graph) and low-WSS (bottom left graph), when compared to straight flow. Adding spiral flow to the posteriorly-directed graft has the opposite effect from that of the laterally-positioned graft. The most notable differences are shown in the high-WSS areas (bottom right), where counter-clockwise direction reduces wall impingement in the lateral and anteriorly-directed grafts, but causing an increase in the area-size of the posteriorly-directed graft. WSS=wall shear stress.
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S0003-4975(19)31414-6
DOI:
https://doi.org/10.1016/j.athoracsur.2019.08.028
Reference:
ATS 33050
To appear in:
The Annals of Thoracic Surgery
Received Date: 18 January 2019 Revised Date:
6 June 2019
Accepted Date: 8 August 2019
Please cite this article as: Zhang PH, Tkatch C, Vainchtein D, Kresh JY, Aortic Hemodynamics of Spiral-Flow-Generated Mechanical Assistance, The Annals of Thoracic Surgery (2019), doi: https:// doi.org/10.1016/j.athoracsur.2019.08.028. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 by The Society of Thoracic Surgeons
Aortic Hemodynamics of Spiral-Flow-Generated Mechanical Assistance Running Head: Spiral Flow Dynamics: MCS to the Aorta
Pablo Huang Zhang, PhD1, Colin Tkatch, MD2, Dmitri Vainchtein, PhD3, J. Yasha Kresh, PhD1,2
1
Department of Cardiothoracic Surgery, Drexel University College of Medicine;
2
Department of Medicine-HUP, IME-University of Pennsylvania
3
C. & J. Nyheim Plasma Institute, Drexel University
Philadelphia, PA, USA
Key Words: Aortic Hemodynamics, Spiral Flow, Computational Fluid Dynamics, Mechanical Circulatory Support, Outflow Graft
Word Count, Abstract: 243 Total: 4,483
Corresponding Author: J. Yasha Kresh, PhD, FACC FAHA Department of Cardiothoracic Surgery Hahnemann University Hospital Drexel University College of Medicine 245 N. 15th Street, Room-6320, Mail Stop#111 Philadelphia, PA 19102 [email protected]
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Abstract Background: Mechanical circulatory support (MCS) devices are being increasingly used as destination therapy in end-stage heart failure patients. Although current devices have significantly improved survival rates, the resulting hemodynamics remains non-physiological. Spiral forms of blood flow are known to exist in the large arteries (e.g., aorta) and serve as a biomimetic-motivation for generating these physiologically-adapted flow regimes. This research aimed to study the potential benefits of generating spiral flow at the MCS outflow graft and the resultant flow-fields in the aorta, including recirculation zones and endothelial wall shear stress (WSS) areas. Methods: A 3D-model of an outflow graft virtually anastomosed end-to-side to an imagederived aortic arch was used in computational fluid dynamic simulations. To study the impact of both spiral flow modulation (clockwise/counter-clockwise helical-flow content) and the outflow graft anastomosis angle (inferiorly/superiorly-directed, anteriorly/posteriorly-directed), flow velocities were measured, low/high-WSS were computed, and fluid streamlines were visualized. Results: Increased helical-flow content reduced regions of low-velocity (<5cm/s), minimized areas exhibiting low-WSS (<3dyn/cm2), and concomitantly increased areas of high-WSS (>80dyn/cm2). The outflow graft anastomosis angle was a key determinant of aortic root washout and fluid-jet wall impingement. Despite counter-clockwise spiral flow predominance in diminishing the size of recirculation/stasis zones compared to straight/clockwise flow, exceptions to this were noted with the superiorly-directed and posteriorly-directed graft placements. Conclusions: Spiral flow-forms better tailored to the underlying three-dimensional aortic curvature and graft angle positioning is expected to help attenuate atherogenesis, preventing vascular remodeling and minimizing plaque formation/erosion in mechanically assisted circulation.
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Heart disease is the leading cause of death in the United States, annually contributing to about a quarter of all deaths nationwide (1). Technological advancements of continuous-flow mechanical circulatory support (MCS) devices for patients with heart failure have increasingly led to their use not only as a bridge-to-transplant, but as a destination therapy (2). While current MCS devices can maintain blood circulation, complications such as bleeding, thromboembolic events, infection, and inflow suction-induced arrhythmias limit optimal outcomes (3, 4). Using biologically-inspired spiral forms of flow, this work explores how the manipulation of MCS outflow characteristics can ameliorate device mediated vascular complications.
Spiral blood flow, consisting of combined axial and circumferential flow fields, has been identified throughout the cardiovascular system and postulated to offer several hemodynamic benefits, including the normalization of wall shear stress (WSS) gradients (5-8). WSS is a fluidvelocity-induced tangential force that plays an important role in endothelial cell mechanosignaling. It is well understood that prolonged exposure to low-WSS induces flow-mediated endothelial cell mis-patterning, leading to increased vascular wall permeability and subsequent atherothrombotic risk/development (9). Conversely, excessively high-WSS can lead to vascular wall fatigue and platelet activation.
Several studies have reported on the benefits of producing/propagating spiral flow in the arterial system. For example, Houston et al. demonstrated that patients with severe renal artery stenosis and decreased native spiral flow prevalence exhibited accelerated progression of renal impairment (10). Chen et al. determined that endovascular stent designs with spiral flow generation promoted the reduction of flow disturbance regions and an increase in average endothelial WSS (11). Using numerical simulations, Deng et al. reported that generation and propagation of spiral flow in the aortic arch reduced luminal surface low-density lipoprotein concentration, limiting the development of atherosclerosis (12). Spiral flow has also been shown
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to reduce platelet adhesion to collagen-coated surfaces in sudden expansion conduit models, without impacting platelet activation potential (13). Finally, spiral flow has been shown to limit energy dissipation and turbulence while reducing areas of recirculation/stasis in stenotic vascular models (14). It is important to also recognize pathological forms of spiral flow; they usually have very short helical wavelengths and can manifest in instances of bicuspid aortic valve (15).
Positioning and angle of the MCS device outflow graft have consequential effects on aortic arch hemodynamics (16, 17). May-Newman et al. used an idealized aorta model and computational fluid dynamic (CFD) approach to show that the outflow graft positioning significantly affected flow disturbance and washout in the aortic arch, especially in patients with diminished native aortic root flow (18). Caruso et al. studied the vertical positioning of the outflow graft and emphasized the importance of balancing flow organization in the aortic arch with disease-prone recirculation regions in the ascending aorta (19). Several studies have shown that a shallow anastomotic angle with respect to the ascending aorta reduced the development of pathologic secondary flow and minimized embolization potential to the cerebral vessels (17, 20, 21).
While several studies have looked at the outflow graft positioning and angle, few have evaluated the aortic hemodynamics of incorporating spiral flow mechanics to the MCS outflow. The presented research aimed to study the biomechanical and hemodynamic impact of spiral forms of flow at the MCS outflow graft – aorta interface. It is well known that the fluid jetting caused by MCS devices drastically alters the aortic flow patterns, introducing pathophysiological flow regimes affecting the vascular response. The effects of the intensity of spiral flow modulation and the insertion angle of the outflow graft were evaluated in terms of previously established benefits: normalization of WSS gradients, diminishing high-velocity jet-flow on the
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vascular wall (impingement), and reduction of regions of low flow. This work is not only expected to inform future MCS device designs by elucidating the beneficial role of spiral flow as an organizational force, but also to provide greater understanding in surgical practice for minimizing progression of flow-induced vascular disease and related adverse clinical outcomes (e.g., intimal hyperplasia, atheroma erosion).
Material and Methods Three computational fluid dynamic (CFD) sub-studies were conducted using a 3Dimage-derived patient aortic arch model, obtained from an online repository (Stratasys, Cambridge, MA). This model was modified using SolidWorks (Dassault Systemes, VelizyVillacoublay, France) to include a laterally-positioned outflow graft (1.6cm diameter) virtually anastomosed end-to-side 2cm below the brachiocephalic trunk (Figure 1). The first sub-study evaluated the effects of spiral flow modulation, introduced at the laterally-positioned outflow graft, on aortic arch hemodynamics. To define the spiral flow intensity, the rotation (revolutions per minute, RPM) and direction (+/- denoting clockwise/counter-clockwise, respectively) of the graft outflow was set to 0, ±70, ±160, ±318, and ±500 RPM. Using straight flow as control and ±160RPM for the spiral flow conditions, the second and third sub-studies evaluated the combined effects of the graft insertion angle and spiral flow content. With respect to the laterally-positioned graft anastomosis (serving as the zero-reference position), the graft was directed inferiorly/superiorly by 20° ( second sub-study), and directed anteriorly/posteriorly by 20° ( third sub-study) (Figure 1).
Computational Fluid Dynamic (CFD) Simulations The open source software OpenFOAM (ESI, Bracknell, UK) was used for the 3D mesh generation and fluid dynamic simulations. The mesh for the aorta model consisted of 1.5 million hexahedral cells. A mesh refinement study was completed using the outflow graft fluid jet
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velocity and the impact WSS as convergence parameters to ensure that the computed results were representative of the flow dynamics (given the geometry and initial conditions) and not due to insufficient analytical-grid resolution of the fluid domain. The working fluid (blood) was modeled as an incompressible Newtonian fluid with a density of 1.06g/cm3 and a viscosity of 4.1cP. A transient solver incorporating turbulence modeling was used to solve the equations (Navier-Stokes) governing fluid dynamics.
No-slip boundary conditions were implemented at all vessel walls, which were assumed to be rigid. Continuous flow 5L/min was generated at the graft simulating MCS outflow, and 1L/min at the aortic root inlet simulating the impaired cardiac output. Spiral flow with variable helical content was implemented at the graft inlet using a rate of rotation (RPM) condition. The 70RPM was chosen to mimic the average human heart rate of 70 beats per minute; 318RPM was used to generate a single helix with a wavelength equivalent to the distance between the modeled graft inlet and the inner curvature of the ascending aorta; 160RPM generated a wavelength twice that of 318RPM; 500RPM generated a wavelength equal to the graft length used in the model (Figure 1). Straight (0 RPM) flow-condition was used at the aortic root inlet boundary and also served as the control-case for the MCS outflow graft.
Analysis and Visualization Post-processing/analysis was conducted using an open-source visualization software (ParaView, Kitware, NY). To evaluate flow disturbance and high-velocity fluid jetting, velocitycolored streamlines and areas of wall shear stress (WSS) were visualized. To quantify and assess the size of atheroprone regions and the impact of high fluid velocity jets, volumes of lowvelocity (<5cm/s), areas of low-WSS (<3dyn/cm2), and areas of high-WSS (>80dyn/cm2) were extracted using threshold analysis methods. The low-WSS cutoff value is associated with
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atherothrombotic risk due to flow-mediated endothelial dysfunction, while the high-WSS value is associated with shear-induced platelet activation.
Results First Sub-Study: Laterally-Positioned Outflow Graft Spiral Flow Modulation The velocity-colored streamlines resulting from the spiral flow modulation at the inlet of the end-to-side, laterally-placed outflow graft are shown in Figure 2. Areas of low-WSS were superimposed on the streamlines to identify regions vulnerable to endothelial dysfunction. Despite the induced straight flow at the graft, the control case exhibited swirling features at the descending aorta, attributed primarily to the additive effects of the aortic arch curvature and three-dimensional torsional geometry of the ascending and descending segments (out-of-plane geometry). The ‘braiding/weaving’ of the streamlines was significantly different for the straight, clockwise, and counter-clockwise flow conditions. As the helical-flow content increased, the high-velocity jetting (red streamlines, Figure 2) at the arch diminished, affecting the size of the recirculation pockets at the descending segment of the aorta. Concurrently, the areas of lowWSS at the aortic root decreased in size with increasing helical-flow content.
Quantitatively, as the helical-flow content increased, the volume of low-velocity in the fluid domain diminished (Figure 3). With the exception of the 500RPM case, counter-clockwise graft flow predominantly minimized regions of low-velocity. With the 500RPM case, clockwise flow decreased the volume of low-velocity by 2.1-fold and counter-clockwise by 1.4-fold, when compared to straight flow.
Spiral flow markedly altered the WSS response, principally decreasing the size of lowWSS area with increasing helical-flow content (Figure 3). At the highest helical-flow content,
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clockwise flow exhibited a 1.5-fold decrease and counter-clockwise flow yielded a 1.2-fold reduction in low-WSS area when compared to straight flow. Despite the reduction of low-WSS areas, higher helical-flow content (e.g., 500RPM) demonstrated increased size of high-WSS areas at the ascending aorta. The highest helical-flow content had on average a 1.3-fold size increase in high-WSS area (actual values exceeding 150dyn/cm2) when compared to straight flow. The 160RPM counter-clockwise flow regime exhibited the smallest area of high-WSS, while also reducing the size of regions with low-velocity and areas of low-WSS. This spiral flow regime was used for two subsequent outflow graft insertion angle variation sub-studies.
Second Sub-Study: Inferiorly/Superiorly-Directed Outflow Graft To study the combined effects of MCS spiral outflow and graft angle variation on aortic hemodynamics, the graft anastomosis angle was directed inferiorly and superiorly (by 20°) with respect to the lateral positioning. The angle of the graft affected the distribution of the highvelocities (colored in red) at the arch and the low-WSS areas at the aortic root (Figure 4). The inferiorly-directed graft had the best clearance of the areas of low-WSS at the root, but caused the high-velocity jets to concentrate on the inner curvature of the ascending aorta creating an impingement force on the wall. The superiorly-directed graft focused high velocities towards the distal wall of the descending aorta, but resulted in the largest areas of low-WSS at the aortic root.
The inferiorly-directed graft anastomosis demonstrated smaller volumes of low-velocity and diminished areas of low-WSS. Straight flow regime for the inferiorly-directed graft had on average a 1.6-fold reduction in low-velocity volume compared to other graft angles (Figure 5). Counter-clockwise graft flow improved predominantly the clearance of low-velocity and lowWSS, and decreased areas of high-WSS created by the fluid-jet impingement, compared to
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straight and clockwise flows. For the inferiorly-directed and lateral grafts, there was a 1.2-fold decrease in low-velocity for counter-clockwise flow compared to straight flow; superiorlydirected graft positioning had a marginal reduction in low-velocity with counter-clockwise flow, compared to straight flow. Although the inferiorly-directed graft positioning was better in diminishing low-WSS areas, it increased the areas of high-WSS, specifically at the fluid jet impact site located contralaterally to the graft outflow (i.e., inner curvature of the arch). However, when compared to straight flow, inducing a clockwise flow in the inferiorly-directed outflow graft yielded a 1.1-fold decrease in size of high-WSS areas, while counter-clockwise flow yielded a 1.4-fold decrease.
Third Sub-Study: Anteriorly/Posteriorly-Directed Outflow Graft The anastomosis angle of the MCS outflow was additionally varied in the transverse plane, directing the graft anteriorly and posteriorly by 20° with respect to the lateral-positioning. In the posteriorly-directed graft, the induced spiral flow increased the size of low-velocity regions and areas of low-WSS (Figure 6). In the anteriorly-directed anastomosis there was no significant improvement in these values with imposed spiral flow. However, high-WSS was significantly affected by varying the transverse angle and adding spiral flow. The anteriorlydirected graft demonstrated a substantially smaller area of high-WSS, where counter-clockwise flow produced a 13.2-fold reduction compared to straight flow. For the posteriorly-directed graft, counter-clockwise flow yielded a 1.15-fold increase in high-WSS area size compared to straight flow. This distinct difference when using counter-clockwise flow can be attributed to the resultant anastomosis-angle-induced fluid jet vascular wall impingement.
Comment The goal of this study was to create an in-silico platform to formulate an integrative understanding of spiral blood flow generated at the MCS outflow graft and the resultant aortic
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hemodynamics. The prevailing three-dimensional curvature of the aorta imparts a natural spiral motion on blood flow which is unique for each patient. These aortic hemodynamic signatures are significantly altered by current MCS devices, which not only extinguish the native spiral flow patterns but also introduce disruptive fluid jets, causing recirculation zones and pathogenic regions of low-WSS, increasing the risk of vascular disease progression and complications (e.g., intimal hyperplasia, atheroma disruption/erosion). The hemodynamic outcomes of introducing spiral flow through an outflow graft, virtually anastomosed end-to-side to the ascending aortic arch of a patient-specific aorta model, were studied in detail.
The first sub-study demonstrated that by increasing the helical-flow content, the high velocities at the arch were diminished and the size of flow recirculation/stasis regions were reduced. The blood transport benefits of spiral flow were similarly observed by others (22, 23). Despite the improvement in areas of low-WSS, increasing helical-flow content (i.e. 500RPM) also increased the areas of WSS in excess of 80dyn/cm2, with overall highest measured peak WSS ~150dyn/cm2. This sub-study provided an important insight on spiral flow generation, establishing that a defined spiral structure (set helical intensity/direction) is not generic, requiring that the 3D vascular geometry of the individual patient should be considered.
In the second sub-study, the inferiorly-directed graft positioning demonstrated the smallest regions of low-velocity and reduced areas of low-WSS, due to the better-aimed washout of the aortic root. However, this configuration also increased the impact area WSS>80dyn/cm2 at the ascending aorta, which was moderated by the imposed spiral flow regimes (i.e., counter-clockwise). While counter-clockwise spiral flow improved overall washout parameters for the inferiorly-directed graft, the superiorly-directed graft fared marginally better with clockwise flow. The difference was largely due to the arch configuration itself; flow from the graft in the superiorly-directed position did not need to navigate the aortic curvature, aiming
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directly towards the descending aorta. Accordingly, the impact WSS areas were the smallest for the superiorly-directed graft.
The third sub-study emphasized the impact of transverse graft positioning on high-WSS areas. As illustrated in Figure 6, the transverse anastomosis placement significantly alters the expected flow trajectory, and consequential mechanical impingement on the wall. The anteriorly-directed graft had a considerably diminished wall impact (impingement) than the laterally-placed graft. The marked decrease in high-WSS in response to the counter-clockwise flow in the anteriorly-directed graft is a reflection of the inherent helical continuity of the fluid structure. This is a striking example of ‘form follows function’, where the modeled threedimensional aortic arch geometry naturally induced a counter-clockwise spiral flow-direction. Clockwise flow in the anteriorly-directed graft increased the wall impact, necessitated by the rotational switch-back (from clockwise to counter-clockwise) dictated by the aortic 3D-curvature. Conversely, the immediacy of the flow impingement on the posterior wall in the posteriorlydirected graft generated increased areas of high-WSS. Given the posterior location of the fluid impact, counter-clockwise graft flow caused the fluid to be forced into the wall, increasing the high-WSS. In this specific case, increasing the helical-flow intensity (higher RPM) in the clockwise direction may help circumnavigate the wall and thus minimize the fluid impact-force.
In evaluating the resultant complex aortic flow dynamics, spiral flow generation was shown to be instrumental in addressing problem regions due to outflow graft fluid jetting. The study provides several translational considerations pertinent to MCS surgical implant approaches. Orienting the MCS outflow graft to the downstream flow is preferable for minimizing areas of high-WSS (associated with vessel wall fatigue/weakening, erosion of pre-existing atheroma and subsequent embolic complication). With limited surgical window and accessibility, the graft placement should be directed to avoid nearby fluid jet impingement on the vascular
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wall. Spiral flow is expected to have broad utility: low helical-flow content can be used to navigate downstream vessel tortuosity in cases where the anastomosis positioning is unrestricted, while high helical-flow content can be used when access is limited and collision of the fluid jet with the vessel wall is unavoidable. Despite the benefits of spiral flow, the jet impact location (anterior/posterior or proximal/distal to the arch) and the preferred fluid-directing rotation of the native aorta should be carefully considered to avoid ‘switch-back’ in spiral directionality, which may contribute to the formation of disturbed flow. Spiral flow must be optimized and informed by the native geometry and flow/anastomosis conditions to prevent detrimental flow-form and vascular-structure mismatching.
There are a number of limitations to numerical modeling in general that need to be acknowledged. In particular, the aortic walls were modeled as rigid boundaries to simplify the chosen computational approach. Although these studies focused on continuous-flow with added spirality, it is important to recognize that in mechanically supported circulation the composite aortic flow preserves some pulsatility. Considering that spiral flow was shown to reduce highvelocity jetting, its role in ameliorating aortic dysfunction (e.g., insufficiency) shows promise and requires further investigation. Importantly, this study was confined to a single aorta model template, and although it did not address the full range of anatomical variations or exhaustively test all the degrees of freedom of the graft anastomosis positions, it created a working framework for testing explicit angles and conditions pertaining to individual surgical cases.
In conclusion, using an in-silico approach, a framework for understanding spiral flow and its associated benefits in assisted circulation was implemented in a patient-derived model of the aortic arch with a virtually anastomosed MCS-pump outflow graft. Specifically, the impact of spiral modulation of the graft outflow and the effect of the graft angle positioning in relation to the ascending aorta were studied. The results demonstrated that increased spiral flow reduced
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regions of low-velocity and areas of low-WSS, important hemodynamic determinants of vascular endothelial dysfunction. When optimized, matching of helical-flow content to the patient-specific vascular anatomy and flow conditions (rotational direction, helical pitch), spiral flow can be used to minimize endothelial-disruption by fluid jetting and improve washout of recirculation/stasis problem zones. Future MCS device designs, incorporating spiral-flow generating features may prove to be a desirable solution improving the hemodynamics of the aorta – outflow graft coupling. Several implantable medical devices (e.g., endovascular grafts, valves, cardiopulmonary bypass cannula) also stand to benefit from spiral flow-induced reduction of fluid flow disturbances and related mechanobiological molecular signaling responses, improving patient-individualized therapy.
Acknowledgement: Aorta model adapted/modified from https://grabcad.com/library/humananatomic-aorta-w-out-extension-1. Computational studies made possible by Proteus, Drexel University’s high-performance computer cluster. Simulation post-processing assistance by Robert Newman. Dmitri Vainchtein supported in part by the National Science Foundation: Award No. CMMI-1740777(D.L.V.).
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References 1.
Heron M. Deaths: Leading causes for 2015. Natl Vital Stat Rep 2017;66(5):1-76.
2.
Pinney SP, Anyanwu AC, Lala A, Teuteberg JJ, Uriel N, Mehra MR. Left ventricular
assist devices for lifelong support. Journal of the American College of Cardiology 2017;69(23):2845-2861. 3.
Slaughter MS, Pagani FD, Rogers JG et al. Clinical management of continuous-flow left
ventricular assist devices in advanced heart failure. The Journal of Heart and Lung Transplantation 2010;29(4, Supplement):S1-S39. 4.
Zhang PH, Kresh JY. Circulatory mechanotherapeutics: Moving with the force. Curr
Cardiol Rep 2018;20(10):94. 5.
Stonebridge PA, Hoskins PR, Allan PL, Belch JF. Spiral laminar flow in vivo. Clin Sci
(Lond) 1996;91(1):17-21. 6.
Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB. Helical and retrograde
secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 1993;88(5 Pt 1):2235-2247. 7.
Frazin LJ, Lanza G, Vonesh M et al. Functional chiral asymmetry in descending thoracic
aorta. Circulation 1990;82(6):1985-1994. 8.
Tanaka M, Sakamoto T, Sugawara S et al. Spiral systolic blood flow in the ascending
aorta and aortic arch analyzed by echo-dynamography. Journal of Cardiology 2010;56(1):97110. 9.
Davies PF. Flow-mediated endothelial mechanotransduction. Physiol Rev
1995;75(3):519-560.
14
10.
Houston JG, Gandy SJ, Milne W, Dick JB, Belch JJ, Stonebridge PA. Spiral laminar flow
in the abdominal aorta: A predictor of renal impairment deterioration in patients with renal artery stenosis? Nephrol Dial Transplant 2004;19(7):1786-1791. 11.
Chen Z, Fan Y, Deng X, Xu Z. Swirling flow can suppress flow disturbances in
endovascular stents: A numerical study. ASAIO journal 2009;55(6):543-549. 12.
Liu X, Pu F, Fan Y, Deng X, Li D, Li S. A numerical study on the flow of blood and the
transport of ldl in the human aorta: The physiological significance of the helical flow in the aortic arch. American Journal of Physiology-Heart and Circulatory Physiology 2009;297(1):H163H170. 13.
Zhan F, Fan Y, Deng X, Xu Z. The beneficial effect of swirling flow on platelet adhesion
to the surface of a sudden tubular expansion tube: Its potential application in end-to-end arterial anastomosis. ASAIO journal 2010;56(3):172-179. 14.
Ha H, Lee SJ. Effect of swirling inlet condition on the flow field in a stenosed arterial
vessel model. Med Eng Phys 2014;36(1):119-128. 15.
Hope MD, Hope TA, Meadows AK et al. Bicuspid aortic valve: Four-dimensional mr
evaluation of ascending aortic systolic flow patterns. Radiology 2010;255(1):53-61. 16.
Litwak KN, Koenig SC, Tsukui H, Kihara Si, Wu Z, Pantalos GM. Effects of left
ventricular assist device support and outflow graft location upon aortic blood flow. ASAIO journal 2004;50(5):432-437. 17.
Chiu WC, Alemu Y, McLarty AJ, Einav S, Slepian MJ, Bluestein D. Ventricular assist
device implantation configurations impact overall mechanical circulatory support system thrombogenic potential. ASAIO journal 2017;63(3):285-292.
15
18.
May-Newman K, Hillen B, Dembitsky W. Effect of left ventricular assist device outflow
conduit anastomosis location on flow patterns in the native aorta. ASAIO journal 2006;52(2):132-139. 19.
Caruso MV, Gramigna V, Rossi M, Serraino GF, Renzulli A, Fragomeni G. A
computational fluid dynamics comparison between different outflow graft anastomosis locations of left ventricular assist device (lvad) in a patient-specific aortic model. International Journal for Numerical Methods in Biomedical Engineering 2015;31(2):e02700. 20.
Argueta-Morales R, Tran R, Ceballos A et al. Mathematical modeling of patient-specific
ventricular assist device implantation to reduce particulate embolization rate to cerebral vessels. Journal of biomechanical engineering 2014;136(7). 21.
Aliseda A, Chivukula VK, McGah P et al. Lvad outflow graft angle and thrombosis risk.
ASAIO journal 2017;63(1):14-23. 22.
Zhang Q, Gao B, Chang Y. Helical flow component of left ventricular assist devices
(lvads) outflow improves aortic hemodynamic states. Medical Science Monitor : International Medical Journal of Experimental and Clinical Research 2018;24:869-879. 23.
Morbiducci U, Gallo D, Cristofanelli S et al. A rational approach to defining principal axes
of multidirectional wall shear stress in realistic vascular geometries, with application to the study of the influence of helical flow on wall shear stress directionality in aorta. J Biomech 2015;48(6):899-906.
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Figure Legends
Figure 1: Model of the patient-specific aorta (right). The outflow graft was virtually anastomosed end-to-side to the ascending aorta in the lateral position. The first sub-study varied the helicalflow content of the outflow graft represented in terms of RPM (left-top, scaled illustration of the theoretical helical wavelength beginning at the graft inlet boundary). The second sub-study varied the anastomosed graft direction inferiorly/superiorly by 20° (left-middle), while the third sub-study directed the graft 20° anteriorly/posteriorly (lef t-bottom). RPM=revolutions/minute.
Figure 2: Velocity-colored streamlines resulting from the spiral flow modulation (clockwise, counter-clockwise) at the inlet of the laterally-placed outflow graft. Regions of WSS<3dyn/cm2 are superimposed to identify atherothrombotic-susceptible areas. Modulation of helical-flow content demonstrates altered fluid jet at the arch and the locality/size of the low-WSS regions. WSS=wall shear stress.
Figure 3: Compared to straight flow, increasing the helical-flow content decreases the volume of low-velocity regions (top). Except for the 500RPM condition, counter-clockwise flow performs better than clockwise flow. Despite smaller areas of low-WSS (bottom left), higher helical-flow content increases the areas of high-WSS (bottom right) at the aortic arch. RPM=revolutions/minute; WSS=wall shear stress.
Figure 4: Velocity-colored streamlines and superimposed WSS<3dyn/cm2 areas resulting from the inferiorly/superiorly-directed graft flow. High velocities (red streamlines) are spatially altered depending on the graft angle: the inferiorly-directed graft causes the fluid jet to impinge on the ascending arch, while the superiorly-directed graft diverts high velocities downstream. The
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inferiorly-directed graft exhibits better aortic root washout, compared to the superiorly-directed graft. RPM=revolutions/minute; WSS=wall shear stress.
Figure 5: The inferiorly-directed graft results in an overall smaller volume of low-velocity (top) and smaller areas of low-WSS (bottom left), but it creates more fluid jetting onto the wall as reflected by the high-WSS areas (bottom right). With the exception of the superiorly-directed graft position, the regions of low-velocity and areas of low-WSS are notably reduced by counterclockwise flow. For high-WSS (>80dyn/cm2), counter-clockwise flow significantly reduces the size of impacted regions. WSS=wall shear stress.
Figure 6: Shown in the left-most column is the top view of the graft flow-trajectory with respect to the transverse anastomosis angle. Adding spiral flow in the anteriorly-directed graft impacts minimally the regions of low-velocity (top graph) and low-WSS (bottom left graph), when compared to straight flow. Adding spiral flow to the posteriorly-directed graft has the opposite effect from that of the laterally-positioned graft. The most notable differences are shown in the high-WSS areas (bottom right), where counter-clockwise direction reduces wall impingement in the lateral and anteriorly-directed grafts, but causing an increase in the area-size of the posteriorly-directed graft. WSS=wall shear stress.
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