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Approaches for treatment of aortic arch aneurysm, a numerical study
Journal of Biomechanics 50 (2017) 158–165
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Approaches for treatment of aortic arch aneurysm, a numerical study Asaph Nardi, Idit Avrahami n Ariel Biomechanics Center, Ariel University, Ariel, Israel
art ic l e i nf o
a b s t r a c t
Article history: Accepted 2 November 2016
Aortic arch aneurysm is a complex pathology which requires coverage of one or more aortic arch vessels. In this study we explore the hemodynamic behavior of the aortic arch in aneurysmatic and treated cases with three currently available treatment approaches: Surgery Graft, hybrid Stent-Graft and chimney Stent Graft. The analysis included four models of the time-dependent fluid domains of aneurysmatic arch and of the surgery, hybrid and chimney endovascular techniques. Dimensions of the models are based on typical anatomy, and boundary conditions are based on typical physiological flow. The simulations used computational fluid dynamics (CFD) methods to delineate the time-dependent flow dynamics in the four geometric models. Results of velocity vectors, flow patterns, blood pressure and wall shear stress distributions are presented. The results delineate disturbed and recirculating flow in the aortic arch aneurysm accompanied with low wall shear stress and velocities, compared to a uniformly directed flow and nominal wall shear stress (WSS) in the model of Surgery graft. Out of the two endograft procedures, the hybrid procedure clearly exhibits better hemodynamic performances over the chimney model, with lower WSS, lower pressure drop and less disturbed and vortical flow regions. Although the chimney procedure requires less manufacturing time and cost, it is associated with higher risk rates, and therefore, it is recommended only for emergency cases. This study may shed light on the hemodynamic factors for these complications and provide insight into ways to improve the procedure. & 2016 Elsevier Ltd. All rights reserved.
Keywords: Thoraces aortic aneurysm Endovascular repair Stent-graft CFD ADINA
1. Introduction Aortic arch aneurysm is a rare condition but carries a high risk of rupture. It enlarges faster and has a higher risk of rupture than other aneurysms. Aneurysmal disease that involves the entire aortic arch is especially prone to extensive involvement because it is a result of diffuse aortic dissection or medial degenerative disease in most cases (Patel and Deeb, 2008). The actuarial 5-year survival of untreated patients is only 13% with many patients dying from aortic rupture. Other severe complications are related to formation of intraluminal thrombus and calcification, which might lead to strokes (Xenos and Bluestein, 2011; Kawatani et al., 2015). The traditional treatment of aortic arch replacement via openchest surgery (Fig. 1b) is a highly complex operation which carries a substantial risk of morbidity and mortality. It requires cardiopulmonary bypass and periods of profound hypothermic circulatory arrest for limiting cerebral metabolism (Ziganshin and n Correspondence to: Department head, Mechanical Engineering and Mechatronics, Ariel University P.O. Box 3, Ariel 44837, Israel. Fax: þ 972 3 9066 652. E-mail address: [email protected] (I. Avrahami).
http://dx.doi.org/10.1016/j.jbiomech.2016.11.038 0021-9290/& 2016 Elsevier Ltd. All rights reserved.
Elefteriades, 2013; Al Kindi et al., 2014). Recent advances in imaging technology and materials technology introduce the endovascular stent graft technology for treatment of aortic pathologies. The use of endovascular stent grafting for repair of aortic aneurysm offers distinct advantages over conventional open surgery as it is deployed under a minimally invasive procedure and without interrupting blood flow. Therefore, it has the potential benefits of greatly reduced risk, a shorter hospital stay, and a more rapid recovery. It is associated with a lower mortality rate, and better short-term performance outcomes (Makaroun et al., 2008; Naughton et al., 2012; Kawatani et al., 2015; Martin et al., 2016). However, the major challenge in endovascular repair of the aortic arch, as in surgical repair, is to maintain blood flow to the brain and side branches in the sealing zone of the stent-graft (Criado et al., 2002). Several approaches were introduced to overcome this challenge. The main two approaches considered are the total hybrid debranching procedures (see Fig. 1c), and the graft procedures using fenestrations or chimney technique (e.g. Chimney of innominate artery, see Fig. 1d). The hybrid total aortic arch debranching (Buth et al., 1998; Gottardi et al., 2005; Saleh and Inglese, 2006; Brinkman et al., 2007) is a combined open heart and endovascular procedure. A bifurcated Dacron graft is connected to the ascending aorta using a proximal end-to-side anastomosis. The
A. Nardi, I. Avrahami / Journal of Biomechanics 50 (2017) 158–165
Aneurysm
Surgery graft
Hybrid stent-graft
Chimney stent-graft
Fig. 1. Schematic illustrations and the geometrical models of the four models: (a) aneurysmatic aortic arch, (b) surgery graft, (c) hybrid graft and (d) chimney stent-graft procedures.
deployment of the endograft is done after bypassing the LSA as shown in Fig. 1c. The graft is custom made in order to minimize interference with the aortic valve and left artery, and thus to fit each individual patient. Although this method requires open surgery to perform the debranching of the supra-aortic vessels, it is considered less invasive and risky when compared to open-chest surgical repair since there is no need for profound hypothermic cardiac arrest (Antoniou et al., 2010; Shirakawa et al., 2013; Zerwes et al., 2015). In the chimney graft technique (Baldwin et al., 2008; Ohrlander et al., 2008; Cires et al., 2011; Moulakakis et al., 2013), a covered stent is deployed parallel to the main aortic stent-graft, protruding somewhat proximally, like a chimney, to preserve flow to a vital side branch, e.g. the Innominate artery (IA), or the left Subclavian artery (LSA). This technique requires two bypass connections between the side branches; e.g., bypass between the IA and the LSA and between the LSA and the left common carotid artery (LCCA), as shown in Fig. 1d. The chimney graft technique allows the use of standard off-the-shelf stent-grafts to instantly treat lesions in aneurysms with challenging neck morphology, providing an alternative to fenestrated stent-grafts in urgent cases. The advantage of chimney repair compared to the other two methods is clear: the stent graft is put into place without open-chest surgery. However, it requires two bypass connections and the entire flow to the upper vessels depends on the single endograft, which is not designed specifically for the anatomic or physiologic conditions found in the arch and its long-term durability remains in question (Yang et al., 2012; Moulakakis et al., 2013). Both endovascular approaches were proven to be technically feasible with high short-term technical success rate and relatively favorable rates of perioperative outcomes (Melissano et al., 2007; Antoniou et al., 2010; Bavaria et al., 2013). Long-term outcomes remain undefined (Szeto et al., 2007; Cires et al., 2011; Yang et al., 2012, Moulakakis et al., 2013; Benrashid et al., 2016). The hybrid technique is considered to have better performance; however it uses custom-made devices associated with long manufacturing times and increased costs (Yoshida et al., 2011; Martin et al., 2016) and is associated with a high reintervention rate due to stentgraft–related complications including migration, endoleaks, stentgraft collapse or fracture, new entry tears or aortic dissection and false lumen thrombosis (Nauta et al., 2015; Benrashid et al., 2016). The chimney technique has the advantage of applying available
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off-the-shelf devices, being technically less complex. In high-risk patients, however, this technique is associated with a relevant morbidity, mortality, and reintervention rate. Therefore, it is often recommended only for patients not suitable for conventional aortic arch repair or emergency cases (Sugiura et al., 2009; Geisbüsch et al., 2011). Blood hemodynamics in the vascular domain has a major role in the disease progression or treatment success. Aneurysmal growth and rupture are strongly correlated with both low and high Wall Shear Stress (WSS) (Feliciani et al., 2015). Vascular regions with disturbed flow accompanied by turbulent flow, low, oscillatory or instantaneous negative WSS and high WSS gradients are strongly correlated with vascular pathologies, cardiovascular diseases, thrombus formation and calcification (Einav and Bluestein, 2004; Reneman et al., 2006; Davies, 2009; Rissland et al., 2009; Tarbell et al., 2014; Zhang et al., 2015). Pressure-related forces are determining factors of drag forces on the stent-grafts leading to stent migration and branches endoleaks or stenosis are often correlated to flow disturbances and small scale vortices in the arterial bypasses (Avrahami et al., 2012). In addition, high velocities have been identified at the stent-graft–induced stenosis of the branches and the distal descending aorta (Wentzel et al., 2005; Canstein et al., 2008; Midulla et al., 2012; van Bogerijen et al., 2014; Nauta et al., 2015). Therefore, a better understanding of the hemodynamic aspects of the different approaches may shed some light on the advantages or complications of each procedure. Computational fluid dynamics (CFD) has been excessively used as a useful tool for exploring of the complex flow mechanics in the aortic arch aneurysm and various treatment approaches in the aortic arch. It was used to analyses and compare the flow patterns, pressure gradients and WSS distribution in the aortic arch, using different flow conditions (Shahcheraghi et al., 2002; Morris et al., 2005; Liu et al., 2009a, 2009b; Liu et al., 2011; Tse et al., 2011; Avrahami, 2013; Avrahami et al., 2013; Markl et al., 2016) before and after treatment for patient specific procedures (Shahcheraghi et al., 2002; Morris et al., 2005; Figueroa et al., 2009; Liu et al., 2009a, 2009b; Tan et al., 2009; Liu et al., 2011; Midulla et al., 2012; Vasava et al., 2012; Konoura et al., 2013; van Bogerijen et al., 2014; Markl et al., 2016) and to analyze drag forces acting on the graft (Lam et al., 2008; Liu et al., 2015). Previous computational studies addressed mostly the fluid dynamics in the aneurysm sac before and after stent grafting, and only few of them addresses chimney endograft procedures. To our knowledge, no investigation was conducted to compare the different endograft approaches from engineering point of view. In this study we use numerical methods to explore and compare the hemodynamic behavior of the aortic arch for aneurysmatic and for these three treatment approaches. 2. Methods The analysis included four models of the time-dependent fluid domains of aneurysmatic arch and of the surgery, hybrid and chimney endovascular techniques (Fig. 1). The flow and pressure fields in the lumen were calculated by numerically solving the momentum and continuity equations for incompressible and Newtonian fluid: DV ∇ U V ¼ 0ρ ¼ ∇p þ μ∇2 V þ ρg Dt
ð1Þ
where p is static pressure, t is time, V is the velocity vector, ρ and μ are density and dynamic viscosity of blood, respectively, and g is the gravity vector. Blood was assumed homogenous, incompressible (with ρ ¼ 1 gr/mL), and Newtonian (with μ ¼ 3.5 cP), and a gravity of g¼ 981 cm/s2 was employed. Flow was assumed laminar. No slip and no penetration boundary conditions were imposed at the grafts and vessels walls (V t ¼ V n ¼ 0). At the aortic inlet, boundary conditions were set according to typical physiological conditions with pulsatile pressure of 120/ 80 mmHg, a heart rate of 75 BPM, and an average cardiac output of CO¼5 L/min
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18mm
6mm
10mm
17mm
8mm 36mm
45mm
35mm
Fig. 2. Models dimensions and the imposed boundary conditions: (a) typical model dimensions, (b) Inlet aortic flow and outlet pressure, as a function of time and (c) flow distribution between side branches. Flow rate at the DA is a resultant (not imposed). (IA- Innominate artery; LSA - left Subclavian artery; LCCA - left common carotid artery; DA - descending aorta).
Aneurysm
Surgery graft
Hybrid stent-graft
Chimney stent-graft
Fig. 3. The four numerically meshed models (top – full models, bottom – magnified view). (shown in Fig. 2b). Flow distribution conditions of 12% to the IA, 8% to the LCCA and 7% to the LSA (Hugo and Michael, 1994) were imposed as described in Fig. 2c. At the du descending aorta outlet, stress-free conditions dx ¼ 0 were prescribed. The timen dependent flow rate at the descending aorta was dictated by mass conservation, leaving about 75% of blood to flow towards lower body. The commercial package SolidWorks (Dassault Systèmes SolidWorks Corp. S. A., France) was used to build the different models, and the commercial package ADINA (ADINA R&D Inc., MA) was used to solve the set of fluid equations and post-process the results. The iterative Generalized Minimal Residual method (GMRES) method was used to solve the system of linear equations. The numerical meshes (Fig. 3) consisted of about 2 M tetrahedral elements each. In order to assess the numerical error of the model, mesh and time-step independence tests were performed on the model of surgery graft. The model was meshed with twelve different mesh resolutions of element size 0.1 cm–0.8 cm (16K–3.9 M tetrahedral elements), and the resulted flow parameters were compared. For example, WSS values during peak flow (t¼ 0.3 s) at the critical point between the IA and the LCCA are compared in Fig. 4 for the twelve mesh models. The model with elements of size 0.13 cm (2,534,198 elements) resulted with an error of 5% in WSS and 0.8% in velocity. For each case, four cardiac cycles were calculated (0 s o to 3.2 s) with total 800 time steps per cycle, using up to 150 iterations in each step. The results of the third cycle were fully periodic (within the error of 1%).
3. Results The resulting velocity flow fields during systole (time ¼2.2 s) as calculated for the four cases are shown as streamlines in Fig. 5.
Fig. 4. Mesh independence test; absolute error calculation in WSS as a function of the number of elements.
Fig. 5a shows flow patterns in the aneurysmatic case. The aneurysm provokes a large recirculation region during the diastole, with a single clear stagnation point. In the surgery graft case (Fig. 5b) smooth flow patterns appear throughout the entire cardiac cycle. In the hybrid graft case during systole (t¼1.9 s) (Fig. 6a), high velocities (440 cm/s) appear in the graft that leads to the LCCA. Elevated velocities are also found in the bypass between the LCCA and the LSA. During diastole (t¼2.2 s) (Fig. 6b and Fig. 5c), noticeable vortices appear at the hybrid graft connection with the ascending aorta. Additional vortices are apparent at the bypass connection between the LCCA and the LSA, at the LSA stump and at the IA curve. In the chimney graft case during systole (t¼1.9 s) (Fig. 7a), high velocities appear in the chimney graft, while peak velocity values (470 cm/s) appear at the bypass between the IA and LCCA. During diastole (t¼ 2.2 s) (Fig. 5d and Fig. 7b), large deceleration vortices appear inside the chimney graft especially near the curved regions. Additional vortices are apparent at the intersection of the chimney stent and the IA, at the bypass connections with the LCCA and LSA and the arterial stumps. A comparison of WSS between the four cases during systole (t¼ 1.9 s) is shown in Fig. 8. In the aneurysm case (Fig. 8a), low WSS ( o2 dyn/cm2) are apparent in the aneurysm region. A local high WSS hotspot ( 16 dyn/cm2) is noticeable at the bottom of the proximal formation bend. In the Surgery graft case (Fig. 8b),
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Aneurysm
Surgery gra
Hybrid stent-gra
161
Chimney stent-gra
Fig. 5. Velocity streamlines in the four models during diastolic phase (time ¼ 2.2 s).
Velocity [cm/s]
Velocity [cm/s]
systole
diastole
Fig. 6. Velocity vectors in the hybrid case at the bypass between the LCCA and LSA (top) and at the anastomosis (bottom), during systole (t ¼1.9 s) (a) and diastole (t¼ 2.2 s) (b).
Velocity [cm/s]
Velocity [cm/s]
the chimney graft (shown in the cut view figure) and at the arterychimney mismatch throughout the IA up to the bypass ( 22 dyn/ cm2) due to the high flow rate in those sections feeding the three arteries. Elevated WSS are also found in the IA - LCCA bypass. In the hybrid graft case (Fig. 8d) higher WSS ( 410 dyn/cm2) appear in the graft that leads to the LCCA and in the bypass between the LCCA and LSA, with peak WSS found near curved regions ( 20 dyn/cm2). In both chimney and hybrid cases, the WSS in the aortic arch are lower than the surgery case, since the flow in the arch in these cases is only 75% of the cardiac output, destined to the descending aorta. The other 25% are diverted upstream to the upper vessels. Thus, the lower flow rate leads to lower WSS. A comparison of pressure distribution during systole (t¼1.9 s) in the four cases is shown in Fig. 9. The cerebral perfusion pressure (CPP) and the aorta-cerebral pressure drop (ΔP) peak during systole in all four models. The pressure increases linearly along the descending aorta due to gravity. Lower pressure values are found at the upper vessels (due to hydrostatic pressure gradients) with pressure drop of about 15 mmHg due to gravity. Since all models are in the same position, the difference in systolic CPP between the four models is a result of hemodynamic viscous losses which are higher for cases with smaller vessels and higher velocities (chimney and hybrid models). Lowest CPP values are found at the upper vessels of the chimney graft case due to a rapid pressure drop ( 45 mmHg) which is a result of the high velocities and disturbed flow in the chimney and bypasses. The critical hemodynamic parameters for the four cases, including maximal velocity, WSS and ΔP during systole (t ¼1.9 s), are summarized in Table 1.
4. Discussion
systole
diastole
Fig. 7. Velocity vectors in the Chimney graft case during systole (t¼ 1.9 s) (a) and diastole (t¼ 2.2 s) (b).
uniform nominal WSS ( o5 dyn/cm2) is found throughout the entire aortic arch, while elevated WSS ( 17 dyn/cm2) is noticeable in the LCCA graft due to high velocities. In the chimney graft case (Fig. 8c) elevated WSS ( 50 dyn/cm2) is apparent especially inside
The disturbed and vortical flow observed in the aneurysm sacs, accompanied with low WSS and stagnant or retrograde velocities, especially during diastole, may imply on pathological hemodynamic characteristics, as pointed out in previous studies ((Di et al., 2001; Steinman et al., 2003; Xenos and Bluestein, 2011), including local stress distribution, complex flow patterns, a large recirculation zone that spans almost the entire diameter of the aneurysmal sac and regions of stagnation that may lead to intraluminal thrombus and anisotropic wall thickness or stiffness. In addition, the non-oriented flows in the aneurysm requires blood to change its direction and velocity on its way downstream. This might
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Shear Stress [dyn/cm2]
Surgery
Aneurysm
Chimney
Hybrid
Fig. 8. Wall shear stress distribution in the aneurysm (a), surgery (b), chimney (c) and hybrid (d) models during systole (t¼ 1.9 s). For the chimney case (c) a mid-plan cut view is also shown to present WSS on the internal covered stent. Gray arrows point regions of interest (see text).
Pressure [dyn/cm2]
Aneurysm
Surgery
Chimney
Hybrid
Fig. 9. Pressure distributions in the four models during systole (t ¼1.9 s). Table 1 Summary of critical hemodynamic parameters during systole (t ¼1.9 s).
Aneurysm Surgery Graft Hybrid SG Chimney SG
Max. velocity [cm/ Pressure drop (ΔP) s] [mmHg]
Max. WSS [dyn/ cm2]
20 25 40 90
16 17 20 50
25 15 31 45
increase risk for wall rupture (Brand et al., 2013; Avrahami et al., 2012). In the surgery case without an aneurysm, the flow field is significantly smoother and particles are well directed towards the branched arteries in a uniform flow profile, even at the last stage of diastole. Out of the two endograft procedures, the hybrid case exhibits better hemodynamic performance, with lower WSS, less vortices and lower pressure drop. The flow in the chimney case is clearly more disturbed, exhibit higher WSS (of up to 50 dyn/cm2 along the chimney graft during peak systole) and the number of local disturbed hemodynamic sites is larger than in the hybrid case due to larger bypass manipulations. Unlike the bifurcated Dacron graft of the hybrid case, the flow inside the chimney-covered stent-graft is characterized with high WSS (50 dyn/cm2), undirected flow due to chimney sharp curvature (as a result of aortic arch anatomic constrictions) and characterized by multiple reverse or vortical flow regions. The extra bypass connection required for the endograft procedures is another source of critical hemodynamic values.
The direction of the bypass connections, especially in the chimney case are imposed by the anatomic configuration of the LSA and IA , resulting in limited bypass flow. The flow in the bypasses is disturbed, especially in the stumps and in the connection to the LSA. As a result, marked pressure drop (up to 45 mmHg) and vortical flow are formed, which might lead to thromboembolism and poor perfusion to the brain and upper body. In comparison, the hybrid case has moderately high WSS ( 20 dyn/cm2) only near curved regions and the major vortex formation near the proximal anastomosis is unstable and temporary, present only during diastole. The pressure drop to the upper vessels of 35 mmHg is 25% higher than the aneurysm case. The chimney procedure also may induce large "gutters", in 7– 15% of the cases (Moulakakis et al., 2013), which allow blood leakage from the endograft sealed zone into the aneurysm, preventing it from clotting and leading to aneurysm progression or rupture (Sugiura et al., 2009; Martin et al., 2016). This issue was not adressed in the present numerical model. The Surgery procedure exhibits clear hemodynamic advantages, in comparison to the other two procedures, with 100% and 200% less pressure drop than the hybrid and chimney cases, correspondingly. It has a uniformly distributed flow and nominal WSS (417 dyn/cm2), therefore, from hemodynamic point of view it has the best performance of all the other cases. Yet, it is considered less favored since it requires open heart surgery during which the patient is hooked up to a cardio-pulmonary bypass pump, put in a hypothermic state under full sedation which result in high mortality and morbidity rates (Stone et al., 2006; Milewski et al., 2010).
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Recently, several alternative approaches are suggested relay on endovascular stent graft designated for the aortic arch, based on a fenestrated primary graft and branches (Yang et al., 2016) or frozen elephant trunk prosthesis(Shrestha et al., 2015). These alternatives still have several challenges to overcome, mainly due to the large anatomical variations, and thus are not in clinical use yet. Among these devices, modular or fenestrated stent grafts designated for the aortic arch (Chuter et al., 2003; Ishimaru, 2004; Sonesson et al., 2009; Yokoi et al., 2013), have the potential to allow hemodynamics similar to the surgery graft, and thus may have an advantage over the endograft procedures in use nowadays.
5. Model limitations and assumptions This study is aimed at comparing the overall behavior of flow in the four cases and thus represents only a quantitative analysis to compare the different procedures. Therefore, the numerical models used several simplifications. Main simplification is related to aortic geometry and boundary conditions. The analyses did not target a specific patient geometry or boundary condition. The models are based on representative prototype anatomical geometry constructed according to a large statistical anatomical database (Hager et al., 2002; Jakanani and Adair, 2010), and the boundary conditions are based on typical time functions garnered from the literature. Since specific patients' anatomy and physiology come in large variations, whatever models we use will lead of inaccuracy for the specific patients, but the typical geometry we chose should be sufficient for a non-specific comparison analysis. In addition, the models ignore the effect of the aortic valve. The aortic valve causes a highly disturbed flow downstream the aorta (Sotiropoulos, 2015) which might influence flow momentum towards the upper vessels and alter the flow patterns, shear stress and pressure distributions in the aortic arch. However, it has a secondary effect on the flow, shear stress and pressure in the upper vessels. We also assumed a vertical (upright) position. It is well known that arterial pressure changes with the body orientation due to hydrostatic pressure gradients (Hill, 1895; Currens, 1948). For example, measurements showed transients of up to 47 mmHg in arterial blood pressure at the level of the carotid by changing orientation (Linnarsson et al., 1996). Similarly, CPP decreases up to 15 mmHg when patients change position from supine (lying down) to upright position (Dawson et al., 2004). Therefore, in order to consider the worst case scenario for the different cases, in this study the upright position was chosen to examine CPP against gravity. The resulted pressure drop due to gravity is about 15 mmHg and the pressure drops due to hemodynamic viscous losses are at the range of 0–30 mmHg (depending on the model). In the case of patient lying down in supine position, CPP should be larger for all cases, while the frictional pressure gradients should not be changed. The assumption of Newtonian fluid should be reasonable in this case, because the shear rates in the aorta are generally greater than 100 s 1 (Fung, 1993). However, the effect of wall motion can be critical, as the motions of the aortic wall were not take into consideration in this study. The effect of wall motion was discussed by previous studies (Jin et al., 2003; van Prehn et al., 2007) and it was suggested that the flow in the aorta is a result not only of aorta geometric curvatures, but also of the motion of the aorta resulting from its attachment to the beating heart. In addition, simulations of aortic hemodynamics with fluid-structure interaction (FSI) approaches were found to predict better the pressure and WSS on the aortic wall (Borghi et al., 2008; Khanafer et al., 2009; Crosetto et al.,
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2011). However, since the mechanical properties of the grafts and the thickness of the aortic wall are in doubt, simulations that include the passive wall motion due to the graft compliance are a great challenge. Therefore, this simplification was inevitable in this case. Another simplification is related to flow assumption. Maximal Reynolds number during peak systole was 1700, and average Reynolds number was 900, thus the simulation used laminar flow models. This assumption may be problematic, since in the aortic arch curvature, the blood flow can undergo a transition from a well-structured laminar state to a chaotic turbulent state during the systolic deceleration phase (Lantz et al., 2013). This transition is a challenge to model. Recent investigations partially succeeded to develop and use low-Reynolds turbulence models that showed good agreements between measurements and numerical results within accuracy of up to 10%. However these models required high computational resources (the simulations required 12 cardiac cycles and mesh sizes of 7 Million elements in order to ensure convergence). These assumptions may lead to some inaccuracies in the values calculated, especially of WSS and pressure. Yet, we believe that our models represent the dominant factors influencing the hemodynamics in the different cases and the simplifications listed above should not change the overall conclusions of the study, which delineates the poor hemodynamics of the aortic arch aneurysm, and presents the hemodynamic advantages of the hybrid procedure over the chimney technique.
6. Conclusions Based on the results presented in this study, surgery graft has the best hemodynamical performance. Out of the two common clinical endograft procedures existing today, the hybrid stent-graft approach has better hemodynamic performance than the chimney procedure. Although the chimney procedure requires less manufacturing time and cost, it is associated with higher risk rates, and therefore, it is recommended only for emergency cases. Improvements in the chimney procedure may take place if the bypass grafts were larger (e.g. 10 mm diameter instead of 8 mm as in the model) and the stumps were shorter or eliminated. The length of the chimney graft should be as short as possible while ensuring graft fixation. The bypass between the LCCA and the LSA should be in the direction of flow as much as possible to reduce the risk of anastomosis failure. The results presented here may shade light on the hemodynamic factors and risk for complications, and provide insight into ways to improve the procedures. In addition, these results may imply that, when approved for clinical use, modular or fenestrated stent grafts designated for the aortic arch may improve the outcomes of endograft procedures in use nowadays.
Conflict of Interest We have no conflict of interest to disclose.
Acknowledgments We wish to thank Ms. Melanie Ratan and Ms. Shirly Steinlauf for their assistance.
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References Al Kindi, A.H., Al Kimyani, N., Alameddine, T., Al Abri, Q., Balan, B., Al Sabti, H., 2014. “Open” approach to aortic arch aneurysm repair. J. Saudi Heart Assoc. 26 (3), 152–161. Antoniou, G., El Sakka, K., Hamady, M., Wolfe, J., 2010. Hybrid treatment of complex aortic arch disease with supra-aortic debranching and endovascular stent graft repair. Eur. J. Vasc. Endovasc. Surg. 39 (6), 683–690. Avrahami, I., 2013. A finite element CFD simulation for predicting patient-specific hemodynamics of an aortic coarctation. International Workshop on Statistical Atlases and Computational Models of the Heart, Springer. Avrahami, I., Brand, M., Meirson, T., OvadiaBlechman, Z., Halak, M., 2012. Hemodynamic and mechanical aspects of fenestrated endografts for treatment of abdominal aortic aneurysm. Eur. J.Mech. B. Fluids 35, 85–91. Avrahami, I., Dilmoney, B., Azuri, A., Brand, M., Cohen, O., Shani, L., Nir, R.R., Bolotin, 2013. Investigation of risks for cerebral embolism associated with the hemodynamics of cardiopulmonary bypass cannula: a numerical model. Artif. Organs 37 (10), 857–865. Baldwin, Z.K., Chuter, T.A., Hiramoto, J.S., Reilly, L.M., Schneider, D.B., 2008. Doublebarrel technique for endovascular exclusion of an aortic arch aneurysm without sternotomy. J. Endovasc. Ther. 15 (2), 161–165. Bavaria, J., Vallabhajosyula, P., Moeller, P., Szeto, W., Desai, N., Pochettino, A., 2013. Hybrid approaches in the treatment of aortic arch aneurysms: postoperative and midterm outcomes. J. Thorac. Cardiovasc. Surg. 145 (3, Supplement), S85–S90. Benrashid, E., Wang, H., Keenan, J.E., Andersen, N.D., Meza, J.M., McCann, R.L., Hughes, G.C., 2016. Evolving practice pattern changes and outcomes in the era of hybrid aortic arch repair. J. Vasc. Surg. 63 (2), 323–331 (e321). Borghi, A., Wood, N.B., Mohiaddin, R.H., Xu, X.Y., 2008. Fluid–solid interaction simulation of flow and stress pattern in thoracoabdominal aneurysms: a patient-specific study. J. Fluids Struct. 24 (2), 270–280. Brand, M., Avrahami, I., Nardi, A., Silverberg, D., Halak, M., 2013 "Clinical, Hemodynamics and Mechanical Aspects of Aortic Aneurisms and Endovascular Repair" in "Aortic Aneurysms: Risk Factors, Diagnosis, Surgery & Repair." ED. Kuivaniemi, H., et al.: Nova Publisher, 181-192. Brinkman, W.T., Szeto, W.Y., Bavaria, J.E., 2007. Stent graft treatment for transverse arch and descending thoracic aorta aneurysms. Curr. Opin. Cardiol. 22 (6), 510. Buth, J., Penn, O., Tielbeek, A., Mersman, M., 1998. Combined approach to stentgraft treatment of an aortic arch aneurysm. J. Endovasc. Ther. 5 (4), 329–332. Canstein, C., Cachot, P., Faust, A., Stalder, A., Bock, J., Frydrychowicz, A., Küffer, J., Hennig, J., Markl, M., 2008. 3D MR flow analysis in realistic rapid‐prototyping model systems of the thoracic aorta: comparison with in vivo data and computational fluid dynamics in identical vessel geometries. Magn. Reson. Med. 59 (3), 535–546. Chuter, T.A.M., Schneider, D.B., Reilly, L.M., Lobo, E.P., Messina, L.M., 2003. Modular branched stent graft for endovascular repair of aortic arch aneurysm and dissection. J. Vasc. Surg. 38 (4), 859–863. Cires, G., Noll, R.E., Albuquerque, F.C., Tonnessen, B.H., Sternbergh, W.C., 2011. Endovascular debranching of the aortic arch during thoracic endograft repair. J. Vasc. Surg. 53 (6), 1485–1491. Criado, F.J., Clark, N.S., Barnatan, M.F., 2002. Stent graft repair in the aortic arch and descending thoracic aorta: a 4-year experience. J. Vasc. Surg. 36 (6), 1121–1128. Crosetto, P., Reymond, P., Deparis, S., Kontaxakis, D., Stergiopulos, N., Quarteroni, A., 2011. Fluid–structure interaction simulation of aortic blood flow. Comput. Fluids 43 (1), 46–57. Currens, J.H., 1948. A comparison of the blood pressure in the lying and standing positions: a study of five hundred men and five hundred women. Am. heart J. 35 (4), 646–654. Davies, P.F., 2009. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc Med 6 (1), 16–26. Dawson, E.A., Secher, N.H., Dalsgaard, M.K., Ogoh, S., Yoshiga, C.C., Gonzalez-Alonso, J., Steensberg, A., Raven, P.B., 2004. Standing up to the challenge of standing: a siphon does not support cerebral blood flow in humans. Am. J. Physiol.-Regul., Integr. Comp. Physiol. 287 (4), R911–R914. Di Martino, E.S., Guadagni, G., Fumero, A., Ballerini, G., Spirito, R., Biglioli, P., Redaelli, A., 2001. Fluid-structure interaction within realistic three-dimensional models of the aneurysmatic aorta as a guidance to assess the risk of rupture of the aneurysm. Med Eng. Phys. 23 (9), 647–655. Einav, S., Bluestein, D., 2004. Dynamics of blood flow and platelet transport in pathological vessels. Card. Eng.: Genes Cells Struct. Funct. 1015, 351–366. Feliciani, G., Potters, W.V., van Ooij, P., Schneiders, J.J., Nederveen, A.J., van Bavel, E., Majoie, C.B., Marquering, H.A., 2015. Multiscale 3-D þ t intracranial aneurysmal flow vortex detection. IEEE Trans. Biomed. Eng. 62 (5), 1355–1362. Figueroa, C.A., Taylor, C.A., Chiou, A.J., Yeh, V., Zarins, C.K., 2009. Magnitude and direction of pulsatile displacement forces acting on thoracic aortic endografts. J. Endovasc. Ther. 16 (3), 350–358. Fung, Y.C. Biomechanics: mechanical properties of living tissues. Springer Science & Business Media, 2013. Geisbüsch, P., Kotelis, D., Müller–Eschner, M., Hyhlik-Dürr, A., Böckler, D., 2011. Complications after aortic arch hybrid repair. J. Vasc. Surg. 53 (4), 935–941. Gottardi, R., Seitelberger, R., Zimpfer, D., Lammer, J., Wolner, E., Grimm, M., Czerny, M., 2005. An alternative approach in treating an aortic arch aneurysm with an anatomic variant by supraaortic reconstruction and stent-graft placement. J. Vasc. Surg. 42 (2), 357–360.
Hager, A., Kaemmerer, H., Rapp-Bernhardt, U., Blücher, S., Rapp, K., Bernhardt, T.M., Galanski, M., Hess, J., 2002. Diameters of the thoracic aorta throughout life as measured with helical computed tomography. J. Thorac. Cardiovasc. Surg. 123 (6), 1060–1066. Hill, L., 1895. The influence of the force of gravity on the circulation of the blood. J. Physiol. 18 (1-2), 15–53. Hugo, G.B., Michael, H.B., 1994. Blood flow measurements in the aorta and major arteries with MR velocity mapping. J. Magn. Reson. Imaging 4 (2), 119–130. Ishimaru, S., 2004. Endografting of the aortic arch. J. Endovasc. Ther. 11 (SupplementII), 62–71. Jakanani, G., Adair, W., 2010. Frequency of variations in aortic arch anatomy depicted on multidetector CT. Clin. Radiol. 65 (6), 481–487. Jin, S., Oshinski, J., Giddens, D.P., 2003. Effects of wall motion and compliance on flow patterns in the ascending aorta. J. Biomech. Eng. 125 (3), 347–354. Kawatani, Y., Hayashi, Y., Ito, Y., Kurobe, H., Nakamura, Y., Suda, Y., Hori, T., 2015. A case of ruptured aortic arch aneurysm successfully treated by thoracic endovascular aneurysm repair with chimney graft. Case Rep. Surg. 2015. Khanafer, K.M., Bull, J.L., Berguer, R., 2009. Fluid-structure interaction of turbulent pulsatile flow within a flexible wall axisymmetric aortic aneurysm model. Eur. J. Mech. - B/Fluids 28 (1), 88–102. Konoura, C., Yagi, T., Nakamura, M., Iwasaki, K., Qian, Y., Okuda, S., Yoshitake, A., Shimizu, H., Yozu, R., Umezu, M., 2013. Numerical analysis of blood flow distribution in 4- and 3-branch vascular grafts. J. Artif. Organs 16 (2), 157–163. Lam, S.K., Fung, G.S.K., Cheng, S.W.K., Chow, K.W., 2008. A computational study on the biomechanical factors related to stent-graft models in the thoracic aorta. Med. Biol. Eng. Comput. 46 (11), 1129–1138. Lantz, J., Ebbers, T., Engvall, J., Karlsson, M., 2013. Numerical and experimental assessment of turbulent kinetic energy in an aortic coarctation. J. Biomech. 46 (11), 1851–1858. Linnarsson, D., Sundberg, C., Tedner, B., Haruna, Y., Karemaker, J., Antonutto, G., Di Prampero, P., 1996. Blood pressure and heart rate responses to sudden changes of gravity during exercise. Am. J. Physiol.-Heart Circ. Physiol. 270 (6), H2132–H2142. Liu, K.-S., Lee, C.-H., Tsai, F.-C., Jhong, G.-H., Hung, K.-C., Liu, S.-J., 2015. Computational analysis of the mechanical behaviors of hemiarch and total arch replacements. Ann. Biomed. Eng. 43 (12), 2881–2891. Liu, X., Fan, Y., Deng, X., Zhan, F., 2011. Effect of non-Newtonian and pulsatile blood flow on mass transport in the human aorta. J. Biomech. 44 (6), 1123–1131. Liu, X., Pu, F., Fan, Y., Deng, X., Li, D., Li, S., 2009a. 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. Am. J. Physiol. - Heart Circ. Physiol. 297 (1), H163–H170. Liu, X., Pu, F., Fan, Y., Deng, X., Li, D., Li, S., 2009b. 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. Am. J. Physiol.-Heart Circ. Physiol. 297 (1), H163. Makaroun, M.S., Dillavou, E.D., Wheatley, G.H., Cambria, R.P., Investigators, G.T., 2008. Five-year results of endovascular treatment with the Gore TAG device compared with open repair of thoracic aortic aneurysms. J. Vasc. Surg. 47 (5), 912–918. Markl, M., Wagner, G.J., Barker, A.J., 2016. Re: blood flow analysis of the aortic arch using computational fluid dynamics, Eur. J. Cardio-Thoracic Surg., pp. 1586–1587, ezv480. Martin, G., Riga, C., Gibbs, R., Jenkins, M., Hamady, M., Bicknell, C., 2016. Short- and long-term results of hybrid arch and proximal descending thoracic aortic repair: a benchmark for new technologies.". J. Endovasc. Ther. 23 (5), 783–790. Melissano, G., Civilini, E., Bertoglio, L., Calliari, F., Setacci, F., Calori, G., Chiesa, R., 2007. Results of endografting of the aortic arch in different landing zones. Eur. J. Vasc. Endovasc. Surg. 33 (5), 561–566. Midulla, M., Moreno, R., Baali, A., Chau, M., Negre-Salvayre, A., Nicoud, F., Pruvo, J.P., Haulon, S., Rousseau, H., 2012. Haemodynamic imaging of thoracic stentgrafts by computational fluid dynamics (CFD): presentation of a patient-specific method combining magnetic resonance imaging and numerical simulations. Eur. Radiol. 22 (10), 2094–2102. Milewski, R.K., Szeto, W.Y., Pochettino, A., Moser, G.W., Moeller, P., Bavaria, J.E., 2010. Have hybrid procedures replaced open aortic arch reconstruction in highrisk patients? A comparative study of elective open arch debranching with endovascular stent graft placement and conventional elective open total and distal aortic arch reconstruction. J. Thorac. Cardiovasc. Surg. 140 (3), 590–597. Morris, L., Delassus, P., Callanan, A., Walsh, M., Wallis, F., Grace, P., McGloughlin, T., 2005. 3-D numerical simulation of blood flow through models of the human aorta. J. Biomech. Eng. 127, 767. Moulakakis, K.G., Mylonas, S.N., Dalainas, I., Sfyroeras, G.S., Markatis, F., Kotsis, T., Kakisis, J., Liapis, C.D., 2013. The chimney-graft technique for preserving supraaortic branches: a review. Ann. Cardiothorac. Surg. 2 (3), 339–346. Naughton, P.A., Park, M.S., Morasch, M.D., Rodriguez, H.E., Garcia-Toca, M., Wang, C. E., Eskandari, M.K., 2012. Emergent repair of acute thoracic aortic catastrophes: a comparative analysis. Arch. Surg. 147 (3), 243–249. Nauta, F.J.H., Conti, M., Kamman, A.V., van Bogerijen, G.H.W., Tolenaar, J.L., Auricchio, F., Figueroa, C.A., van Herwaarden, J.A., Moll, F.L., Trimarchi, S., 2015. Biomechanical changes after thoracic endovascular aortic repair in type B dissection: a systematic review. J. Endovasc. Ther. 22 (6), 918–933. Ohrlander, T., Sonesson, B., Ivancev, K., Resch, T., Dias, N., Malina, M., 2008. The chimney graft: a technique for preserving or rescuing aortic branch vessels in stent-graft sealing zones. J. Endovasc. Ther. 15 (4), 427–432.
A. Nardi, I. Avrahami / Journal of Biomechanics 50 (2017) 158–165
Patel, H.J., Deeb, G.M., 2008. Ascending and arch aorta pathology, natural history, and treatment. Circulation 118 (2), 188–195. Reneman, R.S., Arts, T., Hoeks, A.P., 2006. Wall shear stress–an important determinant of endothelial cell function and structure–in the arterial system in vivo. J. Vasc. Res. 43 (3), 251–269. Rissland, P., Alemu, Y., Einav, S., Ricotta, J., Bluestein, D., 2009. Abdominal aortic aneurysm risk of rupture: patient-specific FSI simulations using anisotropic model. J. Biomech. Eng. 131, 031001. Saleh, H.M., Inglese, L., 2006. Combined surgical and endovascular treatment of aortic arch aneurysms. J. Vasc. Surg. 44 (3), 460–466 (e461). Shahcheraghi, N., Dwyer, H.A., Cheer, A.Y., Barakat, A.I., Rutaganira, T., 2002. Unsteady and three-dimensional simulation of blood flow in the human aortic arch. J. Biomech. Eng. 124, 378. Shirakawa, Y., Kuratani, T., Shimamura, K., Torikai, K., Sakamoto, T., Shijo, T., Sawa, Y., 2015. The efficacy and short-term results of hybrid thoracic endovascular repair into the ascending aorta for aortic arch pathologies. Eur. J. Cardio-Thorac. Surg. 43 (3), 1–11. Shrestha, M., Bachet, J., Bavaria, J., Carrel, T.P., Paulis, R. De, Bartolomeo, R. Di, Etz, C. D., Grabenwöger, M., Grimm, M., Haverich, A., 2015. Current status and recommendations for use of the frozen elephant trunk technique: a position paper by the Vascular Domain of EACTS. Eur. J. Cardio-Thorac. Surg. (ezv085) Sonesson, B., Resch, T., Allers, M., Malina, M., 2009. Endovascular total aortic arch replacement by in situ stent graft fenestration technique. J. Vasc. Surg. 49 (6), 1589–1591. Sotiropoulos, F., 2015. Fluid mechanics of heart valves and their replacements. Annu. Rev. Fluid Mech. 48 (1). Steinman, D.A., Vorp, D.A., Ethier, C.R., 2003. Computational modeling of arterial biomechanics: insights into pathogenesis and treatment of vascular disease. J. Vasc. Surg. 37 (5), 1118–1128. Stone, D.H., Brewster, D.C., Kwolek, C.J., LaMuraglia, G.M., Conrad, M.F., Chung, T.K., Cambria, R.P., 2006. Stent-graft versus open-surgical repair of the thoracic aorta: mid-term results. J. Vasc. Surg. 44 (6), 1188–1197. Sugiura, K., Sonesson, B., Akesson, M., Björses, K., Holst, J., Malina, M., 2009. The applicability of chimney grafts in the aortic arch. J. Cardiovasc. Surg. 50 (4), 475–481. Szeto, W.Y., Bavaria, J.E., Bowen, F.W., Woo, E.Y., Fairman, R.M., Pochettino, A., 2007. The hybrid total arch repair: brachiocephalic bypass and concomitant endovascular aortic arch stent graft placement. J. Card. Surg. 22 (2), 97–102. Tan, F.P.P., Borghi, A., Mohiaddin, R.H., Wood, N.B., Thom, S., Xu, X.Y., 2009. Analysis of flow patterns in a patient-specific thoracic aortic aneurysm model. Comput. Struct. 87 (11–12), 680–690. Tarbell, J.M., Shi, Z.-D., Dunn, J., Jo, H., 2014. Fluid mechanics, arterial disease, and gene expression. Annu. Rev. Fluid Mech. 46, 591–614.
165
Tse, K.M., Chiu, P., Lee, H.P., Ho, P., 2011. Investigation of hemodynamics in the development of dissecting aneurysm within patient-specific dissecting aneurismal aortas using computational fluid dynamics (CFD) simulations. J. Biomech. 44 (5), 827–836. van Bogerijen, G.H.W., Auricchio, F., Conti, M., Lefieux, A., Reali, A., Veneziani, A., Tolenaar, J.L., Moll, F.L., Rampoldi, V., Trimarchi, S., 2014. Aortic hemodynamics after thoracic endovascular aortic repair, with particular attention to the birdbeak configuration. J. Endovasc. Ther. 21 (6), 791–802. van Prehn, J., Vincken, K.L., Muhs, B.E., Barwegen, G.K.W., Bartels, L.W., Prokop, M., Moll, F.L., Verhagen, H.J.M., 2007. Toward endografting of the ascending aorta: insight into dynamics using dynamic cine-CTA. J. Endovasc. Ther. 14 (4), 551–560. Vasava, P., Jalali, P., Dabagh, M., Kolari, P.J., 2012. Finite element modelling of pulsatile blood flow in idealized model of human aortic arch: study of hypotension and hypertension. Comput. Math. Methods Med. 2012. Wentzel, J.J., Corti, R., Fayad, Z.A., Wisdom, P., Macaluso, F., Winkelman, M.O., Fuster, V., Badimon, J.J., 2005. Does shear stress modulate both plaque progression and regression in the thoracic aorta?: human study using serial magnetic resonance imaging. J. Am. Coll. Cardiol. 45 (6), 846–854. Xenos, M., Bluestein, D., 2011. Biomechanical aspects of abdominal aortic aneurysm (AAA) and its risk of rupture: fluid structure interaction (FSI) studies. Biomech. Mechanobiol. Aneurysms, 181–220. Yang, J., Liu, Y., Duan, W., Yi, D., Yu, S., Ma, R., Ren, J., 2016. A feasibility study of total endovascular aortic arch replacement: from stent-graft design to preclinical testing. J. Thorac. Cardiovasc. Surg. 151 (4), 1203–1212. Yang, J., Xiong, J., Liu, X., Jia, X., Zhu, Y., Guo, W., 2012. Endovascular chimney technique of aortic arch pathologies: a systematic review. Ann. Vasc. Surg. 26 (7), 1014–1021. Yokoi, Y., Azuma, T., Yamazaki, K., 2013. Advantage of a precurved fenestrated endograft for aortic arch disease: simplified arch aneurysm treatment in Japan 2010 and 2011. J. Thorac. Cardiovasc. Surg. 145 (3, Supplement), S103–S109. Yoshida, R., Kolvenbach, R., Yoshida, W., Wassijew, S., Schwierz, E., Lin, F., 2011. Total endovascular debranching of the aortic arch. Eur. J. Vasc. Endovasc. Surg. 42 (5), 627–630. Zerwes, S., Leissner, G., Gosslau, Y., Jakob, R., Bruijnen, H.-K., Oertl, F., Woelfle, K., 2015. Clinical outcomes in hybrid repair procedures for pathologies involving the aortic arch. Vascular 23 (1), 9–16. Zhang, P., Liu, X., Sun, A., Fan, Y., Deng, X., 2015. Hemodynamic insight into overlapping bare-metal stents strategy in the treatment of aortic aneurysm. J. Biomech. 48 (10), 2041–2046. Ziganshin, B.A., Elefteriades, J.A., 2013. Deep hypothermic circulatory arrest. Ann. Cardiothorac. Surg. 2 (3), 303–315.
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Approaches for treatment of aortic arch aneurysm, a numerical study Asaph Nardi, Idit Avrahami n Ariel Biomechanics Center, Ariel University, Ariel, Israel
art ic l e i nf o
a b s t r a c t
Article history: Accepted 2 November 2016
Aortic arch aneurysm is a complex pathology which requires coverage of one or more aortic arch vessels. In this study we explore the hemodynamic behavior of the aortic arch in aneurysmatic and treated cases with three currently available treatment approaches: Surgery Graft, hybrid Stent-Graft and chimney Stent Graft. The analysis included four models of the time-dependent fluid domains of aneurysmatic arch and of the surgery, hybrid and chimney endovascular techniques. Dimensions of the models are based on typical anatomy, and boundary conditions are based on typical physiological flow. The simulations used computational fluid dynamics (CFD) methods to delineate the time-dependent flow dynamics in the four geometric models. Results of velocity vectors, flow patterns, blood pressure and wall shear stress distributions are presented. The results delineate disturbed and recirculating flow in the aortic arch aneurysm accompanied with low wall shear stress and velocities, compared to a uniformly directed flow and nominal wall shear stress (WSS) in the model of Surgery graft. Out of the two endograft procedures, the hybrid procedure clearly exhibits better hemodynamic performances over the chimney model, with lower WSS, lower pressure drop and less disturbed and vortical flow regions. Although the chimney procedure requires less manufacturing time and cost, it is associated with higher risk rates, and therefore, it is recommended only for emergency cases. This study may shed light on the hemodynamic factors for these complications and provide insight into ways to improve the procedure. & 2016 Elsevier Ltd. All rights reserved.
Keywords: Thoraces aortic aneurysm Endovascular repair Stent-graft CFD ADINA
1. Introduction Aortic arch aneurysm is a rare condition but carries a high risk of rupture. It enlarges faster and has a higher risk of rupture than other aneurysms. Aneurysmal disease that involves the entire aortic arch is especially prone to extensive involvement because it is a result of diffuse aortic dissection or medial degenerative disease in most cases (Patel and Deeb, 2008). The actuarial 5-year survival of untreated patients is only 13% with many patients dying from aortic rupture. Other severe complications are related to formation of intraluminal thrombus and calcification, which might lead to strokes (Xenos and Bluestein, 2011; Kawatani et al., 2015). The traditional treatment of aortic arch replacement via openchest surgery (Fig. 1b) is a highly complex operation which carries a substantial risk of morbidity and mortality. It requires cardiopulmonary bypass and periods of profound hypothermic circulatory arrest for limiting cerebral metabolism (Ziganshin and n Correspondence to: Department head, Mechanical Engineering and Mechatronics, Ariel University P.O. Box 3, Ariel 44837, Israel. Fax: þ 972 3 9066 652. E-mail address: [email protected] (I. Avrahami).
http://dx.doi.org/10.1016/j.jbiomech.2016.11.038 0021-9290/& 2016 Elsevier Ltd. All rights reserved.
Elefteriades, 2013; Al Kindi et al., 2014). Recent advances in imaging technology and materials technology introduce the endovascular stent graft technology for treatment of aortic pathologies. The use of endovascular stent grafting for repair of aortic aneurysm offers distinct advantages over conventional open surgery as it is deployed under a minimally invasive procedure and without interrupting blood flow. Therefore, it has the potential benefits of greatly reduced risk, a shorter hospital stay, and a more rapid recovery. It is associated with a lower mortality rate, and better short-term performance outcomes (Makaroun et al., 2008; Naughton et al., 2012; Kawatani et al., 2015; Martin et al., 2016). However, the major challenge in endovascular repair of the aortic arch, as in surgical repair, is to maintain blood flow to the brain and side branches in the sealing zone of the stent-graft (Criado et al., 2002). Several approaches were introduced to overcome this challenge. The main two approaches considered are the total hybrid debranching procedures (see Fig. 1c), and the graft procedures using fenestrations or chimney technique (e.g. Chimney of innominate artery, see Fig. 1d). The hybrid total aortic arch debranching (Buth et al., 1998; Gottardi et al., 2005; Saleh and Inglese, 2006; Brinkman et al., 2007) is a combined open heart and endovascular procedure. A bifurcated Dacron graft is connected to the ascending aorta using a proximal end-to-side anastomosis. The
A. Nardi, I. Avrahami / Journal of Biomechanics 50 (2017) 158–165
Aneurysm
Surgery graft
Hybrid stent-graft
Chimney stent-graft
Fig. 1. Schematic illustrations and the geometrical models of the four models: (a) aneurysmatic aortic arch, (b) surgery graft, (c) hybrid graft and (d) chimney stent-graft procedures.
deployment of the endograft is done after bypassing the LSA as shown in Fig. 1c. The graft is custom made in order to minimize interference with the aortic valve and left artery, and thus to fit each individual patient. Although this method requires open surgery to perform the debranching of the supra-aortic vessels, it is considered less invasive and risky when compared to open-chest surgical repair since there is no need for profound hypothermic cardiac arrest (Antoniou et al., 2010; Shirakawa et al., 2013; Zerwes et al., 2015). In the chimney graft technique (Baldwin et al., 2008; Ohrlander et al., 2008; Cires et al., 2011; Moulakakis et al., 2013), a covered stent is deployed parallel to the main aortic stent-graft, protruding somewhat proximally, like a chimney, to preserve flow to a vital side branch, e.g. the Innominate artery (IA), or the left Subclavian artery (LSA). This technique requires two bypass connections between the side branches; e.g., bypass between the IA and the LSA and between the LSA and the left common carotid artery (LCCA), as shown in Fig. 1d. The chimney graft technique allows the use of standard off-the-shelf stent-grafts to instantly treat lesions in aneurysms with challenging neck morphology, providing an alternative to fenestrated stent-grafts in urgent cases. The advantage of chimney repair compared to the other two methods is clear: the stent graft is put into place without open-chest surgery. However, it requires two bypass connections and the entire flow to the upper vessels depends on the single endograft, which is not designed specifically for the anatomic or physiologic conditions found in the arch and its long-term durability remains in question (Yang et al., 2012; Moulakakis et al., 2013). Both endovascular approaches were proven to be technically feasible with high short-term technical success rate and relatively favorable rates of perioperative outcomes (Melissano et al., 2007; Antoniou et al., 2010; Bavaria et al., 2013). Long-term outcomes remain undefined (Szeto et al., 2007; Cires et al., 2011; Yang et al., 2012, Moulakakis et al., 2013; Benrashid et al., 2016). The hybrid technique is considered to have better performance; however it uses custom-made devices associated with long manufacturing times and increased costs (Yoshida et al., 2011; Martin et al., 2016) and is associated with a high reintervention rate due to stentgraft–related complications including migration, endoleaks, stentgraft collapse or fracture, new entry tears or aortic dissection and false lumen thrombosis (Nauta et al., 2015; Benrashid et al., 2016). The chimney technique has the advantage of applying available
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off-the-shelf devices, being technically less complex. In high-risk patients, however, this technique is associated with a relevant morbidity, mortality, and reintervention rate. Therefore, it is often recommended only for patients not suitable for conventional aortic arch repair or emergency cases (Sugiura et al., 2009; Geisbüsch et al., 2011). Blood hemodynamics in the vascular domain has a major role in the disease progression or treatment success. Aneurysmal growth and rupture are strongly correlated with both low and high Wall Shear Stress (WSS) (Feliciani et al., 2015). Vascular regions with disturbed flow accompanied by turbulent flow, low, oscillatory or instantaneous negative WSS and high WSS gradients are strongly correlated with vascular pathologies, cardiovascular diseases, thrombus formation and calcification (Einav and Bluestein, 2004; Reneman et al., 2006; Davies, 2009; Rissland et al., 2009; Tarbell et al., 2014; Zhang et al., 2015). Pressure-related forces are determining factors of drag forces on the stent-grafts leading to stent migration and branches endoleaks or stenosis are often correlated to flow disturbances and small scale vortices in the arterial bypasses (Avrahami et al., 2012). In addition, high velocities have been identified at the stent-graft–induced stenosis of the branches and the distal descending aorta (Wentzel et al., 2005; Canstein et al., 2008; Midulla et al., 2012; van Bogerijen et al., 2014; Nauta et al., 2015). Therefore, a better understanding of the hemodynamic aspects of the different approaches may shed some light on the advantages or complications of each procedure. Computational fluid dynamics (CFD) has been excessively used as a useful tool for exploring of the complex flow mechanics in the aortic arch aneurysm and various treatment approaches in the aortic arch. It was used to analyses and compare the flow patterns, pressure gradients and WSS distribution in the aortic arch, using different flow conditions (Shahcheraghi et al., 2002; Morris et al., 2005; Liu et al., 2009a, 2009b; Liu et al., 2011; Tse et al., 2011; Avrahami, 2013; Avrahami et al., 2013; Markl et al., 2016) before and after treatment for patient specific procedures (Shahcheraghi et al., 2002; Morris et al., 2005; Figueroa et al., 2009; Liu et al., 2009a, 2009b; Tan et al., 2009; Liu et al., 2011; Midulla et al., 2012; Vasava et al., 2012; Konoura et al., 2013; van Bogerijen et al., 2014; Markl et al., 2016) and to analyze drag forces acting on the graft (Lam et al., 2008; Liu et al., 2015). Previous computational studies addressed mostly the fluid dynamics in the aneurysm sac before and after stent grafting, and only few of them addresses chimney endograft procedures. To our knowledge, no investigation was conducted to compare the different endograft approaches from engineering point of view. In this study we use numerical methods to explore and compare the hemodynamic behavior of the aortic arch for aneurysmatic and for these three treatment approaches. 2. Methods The analysis included four models of the time-dependent fluid domains of aneurysmatic arch and of the surgery, hybrid and chimney endovascular techniques (Fig. 1). The flow and pressure fields in the lumen were calculated by numerically solving the momentum and continuity equations for incompressible and Newtonian fluid: DV ∇ U V ¼ 0ρ ¼ ∇p þ μ∇2 V þ ρg Dt
ð1Þ
where p is static pressure, t is time, V is the velocity vector, ρ and μ are density and dynamic viscosity of blood, respectively, and g is the gravity vector. Blood was assumed homogenous, incompressible (with ρ ¼ 1 gr/mL), and Newtonian (with μ ¼ 3.5 cP), and a gravity of g¼ 981 cm/s2 was employed. Flow was assumed laminar. No slip and no penetration boundary conditions were imposed at the grafts and vessels walls (V t ¼ V n ¼ 0). At the aortic inlet, boundary conditions were set according to typical physiological conditions with pulsatile pressure of 120/ 80 mmHg, a heart rate of 75 BPM, and an average cardiac output of CO¼5 L/min
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18mm
6mm
10mm
17mm
8mm 36mm
45mm
35mm
Fig. 2. Models dimensions and the imposed boundary conditions: (a) typical model dimensions, (b) Inlet aortic flow and outlet pressure, as a function of time and (c) flow distribution between side branches. Flow rate at the DA is a resultant (not imposed). (IA- Innominate artery; LSA - left Subclavian artery; LCCA - left common carotid artery; DA - descending aorta).
Aneurysm
Surgery graft
Hybrid stent-graft
Chimney stent-graft
Fig. 3. The four numerically meshed models (top – full models, bottom – magnified view). (shown in Fig. 2b). Flow distribution conditions of 12% to the IA, 8% to the LCCA and 7% to the LSA (Hugo and Michael, 1994) were imposed as described in Fig. 2c. At the du descending aorta outlet, stress-free conditions dx ¼ 0 were prescribed. The timen dependent flow rate at the descending aorta was dictated by mass conservation, leaving about 75% of blood to flow towards lower body. The commercial package SolidWorks (Dassault Systèmes SolidWorks Corp. S. A., France) was used to build the different models, and the commercial package ADINA (ADINA R&D Inc., MA) was used to solve the set of fluid equations and post-process the results. The iterative Generalized Minimal Residual method (GMRES) method was used to solve the system of linear equations. The numerical meshes (Fig. 3) consisted of about 2 M tetrahedral elements each. In order to assess the numerical error of the model, mesh and time-step independence tests were performed on the model of surgery graft. The model was meshed with twelve different mesh resolutions of element size 0.1 cm–0.8 cm (16K–3.9 M tetrahedral elements), and the resulted flow parameters were compared. For example, WSS values during peak flow (t¼ 0.3 s) at the critical point between the IA and the LCCA are compared in Fig. 4 for the twelve mesh models. The model with elements of size 0.13 cm (2,534,198 elements) resulted with an error of 5% in WSS and 0.8% in velocity. For each case, four cardiac cycles were calculated (0 s o to 3.2 s) with total 800 time steps per cycle, using up to 150 iterations in each step. The results of the third cycle were fully periodic (within the error of 1%).
3. Results The resulting velocity flow fields during systole (time ¼2.2 s) as calculated for the four cases are shown as streamlines in Fig. 5.
Fig. 4. Mesh independence test; absolute error calculation in WSS as a function of the number of elements.
Fig. 5a shows flow patterns in the aneurysmatic case. The aneurysm provokes a large recirculation region during the diastole, with a single clear stagnation point. In the surgery graft case (Fig. 5b) smooth flow patterns appear throughout the entire cardiac cycle. In the hybrid graft case during systole (t¼1.9 s) (Fig. 6a), high velocities (440 cm/s) appear in the graft that leads to the LCCA. Elevated velocities are also found in the bypass between the LCCA and the LSA. During diastole (t¼2.2 s) (Fig. 6b and Fig. 5c), noticeable vortices appear at the hybrid graft connection with the ascending aorta. Additional vortices are apparent at the bypass connection between the LCCA and the LSA, at the LSA stump and at the IA curve. In the chimney graft case during systole (t¼1.9 s) (Fig. 7a), high velocities appear in the chimney graft, while peak velocity values (470 cm/s) appear at the bypass between the IA and LCCA. During diastole (t¼ 2.2 s) (Fig. 5d and Fig. 7b), large deceleration vortices appear inside the chimney graft especially near the curved regions. Additional vortices are apparent at the intersection of the chimney stent and the IA, at the bypass connections with the LCCA and LSA and the arterial stumps. A comparison of WSS between the four cases during systole (t¼ 1.9 s) is shown in Fig. 8. In the aneurysm case (Fig. 8a), low WSS ( o2 dyn/cm2) are apparent in the aneurysm region. A local high WSS hotspot ( 16 dyn/cm2) is noticeable at the bottom of the proximal formation bend. In the Surgery graft case (Fig. 8b),
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Aneurysm
Surgery gra
Hybrid stent-gra
161
Chimney stent-gra
Fig. 5. Velocity streamlines in the four models during diastolic phase (time ¼ 2.2 s).
Velocity [cm/s]
Velocity [cm/s]
systole
diastole
Fig. 6. Velocity vectors in the hybrid case at the bypass between the LCCA and LSA (top) and at the anastomosis (bottom), during systole (t ¼1.9 s) (a) and diastole (t¼ 2.2 s) (b).
Velocity [cm/s]
Velocity [cm/s]
the chimney graft (shown in the cut view figure) and at the arterychimney mismatch throughout the IA up to the bypass ( 22 dyn/ cm2) due to the high flow rate in those sections feeding the three arteries. Elevated WSS are also found in the IA - LCCA bypass. In the hybrid graft case (Fig. 8d) higher WSS ( 410 dyn/cm2) appear in the graft that leads to the LCCA and in the bypass between the LCCA and LSA, with peak WSS found near curved regions ( 20 dyn/cm2). In both chimney and hybrid cases, the WSS in the aortic arch are lower than the surgery case, since the flow in the arch in these cases is only 75% of the cardiac output, destined to the descending aorta. The other 25% are diverted upstream to the upper vessels. Thus, the lower flow rate leads to lower WSS. A comparison of pressure distribution during systole (t¼1.9 s) in the four cases is shown in Fig. 9. The cerebral perfusion pressure (CPP) and the aorta-cerebral pressure drop (ΔP) peak during systole in all four models. The pressure increases linearly along the descending aorta due to gravity. Lower pressure values are found at the upper vessels (due to hydrostatic pressure gradients) with pressure drop of about 15 mmHg due to gravity. Since all models are in the same position, the difference in systolic CPP between the four models is a result of hemodynamic viscous losses which are higher for cases with smaller vessels and higher velocities (chimney and hybrid models). Lowest CPP values are found at the upper vessels of the chimney graft case due to a rapid pressure drop ( 45 mmHg) which is a result of the high velocities and disturbed flow in the chimney and bypasses. The critical hemodynamic parameters for the four cases, including maximal velocity, WSS and ΔP during systole (t ¼1.9 s), are summarized in Table 1.
4. Discussion
systole
diastole
Fig. 7. Velocity vectors in the Chimney graft case during systole (t¼ 1.9 s) (a) and diastole (t¼ 2.2 s) (b).
uniform nominal WSS ( o5 dyn/cm2) is found throughout the entire aortic arch, while elevated WSS ( 17 dyn/cm2) is noticeable in the LCCA graft due to high velocities. In the chimney graft case (Fig. 8c) elevated WSS ( 50 dyn/cm2) is apparent especially inside
The disturbed and vortical flow observed in the aneurysm sacs, accompanied with low WSS and stagnant or retrograde velocities, especially during diastole, may imply on pathological hemodynamic characteristics, as pointed out in previous studies ((Di et al., 2001; Steinman et al., 2003; Xenos and Bluestein, 2011), including local stress distribution, complex flow patterns, a large recirculation zone that spans almost the entire diameter of the aneurysmal sac and regions of stagnation that may lead to intraluminal thrombus and anisotropic wall thickness or stiffness. In addition, the non-oriented flows in the aneurysm requires blood to change its direction and velocity on its way downstream. This might
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Shear Stress [dyn/cm2]
Surgery
Aneurysm
Chimney
Hybrid
Fig. 8. Wall shear stress distribution in the aneurysm (a), surgery (b), chimney (c) and hybrid (d) models during systole (t¼ 1.9 s). For the chimney case (c) a mid-plan cut view is also shown to present WSS on the internal covered stent. Gray arrows point regions of interest (see text).
Pressure [dyn/cm2]
Aneurysm
Surgery
Chimney
Hybrid
Fig. 9. Pressure distributions in the four models during systole (t ¼1.9 s). Table 1 Summary of critical hemodynamic parameters during systole (t ¼1.9 s).
Aneurysm Surgery Graft Hybrid SG Chimney SG
Max. velocity [cm/ Pressure drop (ΔP) s] [mmHg]
Max. WSS [dyn/ cm2]
20 25 40 90
16 17 20 50
25 15 31 45
increase risk for wall rupture (Brand et al., 2013; Avrahami et al., 2012). In the surgery case without an aneurysm, the flow field is significantly smoother and particles are well directed towards the branched arteries in a uniform flow profile, even at the last stage of diastole. Out of the two endograft procedures, the hybrid case exhibits better hemodynamic performance, with lower WSS, less vortices and lower pressure drop. The flow in the chimney case is clearly more disturbed, exhibit higher WSS (of up to 50 dyn/cm2 along the chimney graft during peak systole) and the number of local disturbed hemodynamic sites is larger than in the hybrid case due to larger bypass manipulations. Unlike the bifurcated Dacron graft of the hybrid case, the flow inside the chimney-covered stent-graft is characterized with high WSS (50 dyn/cm2), undirected flow due to chimney sharp curvature (as a result of aortic arch anatomic constrictions) and characterized by multiple reverse or vortical flow regions. The extra bypass connection required for the endograft procedures is another source of critical hemodynamic values.
The direction of the bypass connections, especially in the chimney case are imposed by the anatomic configuration of the LSA and IA , resulting in limited bypass flow. The flow in the bypasses is disturbed, especially in the stumps and in the connection to the LSA. As a result, marked pressure drop (up to 45 mmHg) and vortical flow are formed, which might lead to thromboembolism and poor perfusion to the brain and upper body. In comparison, the hybrid case has moderately high WSS ( 20 dyn/cm2) only near curved regions and the major vortex formation near the proximal anastomosis is unstable and temporary, present only during diastole. The pressure drop to the upper vessels of 35 mmHg is 25% higher than the aneurysm case. The chimney procedure also may induce large "gutters", in 7– 15% of the cases (Moulakakis et al., 2013), which allow blood leakage from the endograft sealed zone into the aneurysm, preventing it from clotting and leading to aneurysm progression or rupture (Sugiura et al., 2009; Martin et al., 2016). This issue was not adressed in the present numerical model. The Surgery procedure exhibits clear hemodynamic advantages, in comparison to the other two procedures, with 100% and 200% less pressure drop than the hybrid and chimney cases, correspondingly. It has a uniformly distributed flow and nominal WSS (417 dyn/cm2), therefore, from hemodynamic point of view it has the best performance of all the other cases. Yet, it is considered less favored since it requires open heart surgery during which the patient is hooked up to a cardio-pulmonary bypass pump, put in a hypothermic state under full sedation which result in high mortality and morbidity rates (Stone et al., 2006; Milewski et al., 2010).
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Recently, several alternative approaches are suggested relay on endovascular stent graft designated for the aortic arch, based on a fenestrated primary graft and branches (Yang et al., 2016) or frozen elephant trunk prosthesis(Shrestha et al., 2015). These alternatives still have several challenges to overcome, mainly due to the large anatomical variations, and thus are not in clinical use yet. Among these devices, modular or fenestrated stent grafts designated for the aortic arch (Chuter et al., 2003; Ishimaru, 2004; Sonesson et al., 2009; Yokoi et al., 2013), have the potential to allow hemodynamics similar to the surgery graft, and thus may have an advantage over the endograft procedures in use nowadays.
5. Model limitations and assumptions This study is aimed at comparing the overall behavior of flow in the four cases and thus represents only a quantitative analysis to compare the different procedures. Therefore, the numerical models used several simplifications. Main simplification is related to aortic geometry and boundary conditions. The analyses did not target a specific patient geometry or boundary condition. The models are based on representative prototype anatomical geometry constructed according to a large statistical anatomical database (Hager et al., 2002; Jakanani and Adair, 2010), and the boundary conditions are based on typical time functions garnered from the literature. Since specific patients' anatomy and physiology come in large variations, whatever models we use will lead of inaccuracy for the specific patients, but the typical geometry we chose should be sufficient for a non-specific comparison analysis. In addition, the models ignore the effect of the aortic valve. The aortic valve causes a highly disturbed flow downstream the aorta (Sotiropoulos, 2015) which might influence flow momentum towards the upper vessels and alter the flow patterns, shear stress and pressure distributions in the aortic arch. However, it has a secondary effect on the flow, shear stress and pressure in the upper vessels. We also assumed a vertical (upright) position. It is well known that arterial pressure changes with the body orientation due to hydrostatic pressure gradients (Hill, 1895; Currens, 1948). For example, measurements showed transients of up to 47 mmHg in arterial blood pressure at the level of the carotid by changing orientation (Linnarsson et al., 1996). Similarly, CPP decreases up to 15 mmHg when patients change position from supine (lying down) to upright position (Dawson et al., 2004). Therefore, in order to consider the worst case scenario for the different cases, in this study the upright position was chosen to examine CPP against gravity. The resulted pressure drop due to gravity is about 15 mmHg and the pressure drops due to hemodynamic viscous losses are at the range of 0–30 mmHg (depending on the model). In the case of patient lying down in supine position, CPP should be larger for all cases, while the frictional pressure gradients should not be changed. The assumption of Newtonian fluid should be reasonable in this case, because the shear rates in the aorta are generally greater than 100 s 1 (Fung, 1993). However, the effect of wall motion can be critical, as the motions of the aortic wall were not take into consideration in this study. The effect of wall motion was discussed by previous studies (Jin et al., 2003; van Prehn et al., 2007) and it was suggested that the flow in the aorta is a result not only of aorta geometric curvatures, but also of the motion of the aorta resulting from its attachment to the beating heart. In addition, simulations of aortic hemodynamics with fluid-structure interaction (FSI) approaches were found to predict better the pressure and WSS on the aortic wall (Borghi et al., 2008; Khanafer et al., 2009; Crosetto et al.,
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2011). However, since the mechanical properties of the grafts and the thickness of the aortic wall are in doubt, simulations that include the passive wall motion due to the graft compliance are a great challenge. Therefore, this simplification was inevitable in this case. Another simplification is related to flow assumption. Maximal Reynolds number during peak systole was 1700, and average Reynolds number was 900, thus the simulation used laminar flow models. This assumption may be problematic, since in the aortic arch curvature, the blood flow can undergo a transition from a well-structured laminar state to a chaotic turbulent state during the systolic deceleration phase (Lantz et al., 2013). This transition is a challenge to model. Recent investigations partially succeeded to develop and use low-Reynolds turbulence models that showed good agreements between measurements and numerical results within accuracy of up to 10%. However these models required high computational resources (the simulations required 12 cardiac cycles and mesh sizes of 7 Million elements in order to ensure convergence). These assumptions may lead to some inaccuracies in the values calculated, especially of WSS and pressure. Yet, we believe that our models represent the dominant factors influencing the hemodynamics in the different cases and the simplifications listed above should not change the overall conclusions of the study, which delineates the poor hemodynamics of the aortic arch aneurysm, and presents the hemodynamic advantages of the hybrid procedure over the chimney technique.
6. Conclusions Based on the results presented in this study, surgery graft has the best hemodynamical performance. Out of the two common clinical endograft procedures existing today, the hybrid stent-graft approach has better hemodynamic performance than the chimney procedure. Although the chimney procedure requires less manufacturing time and cost, it is associated with higher risk rates, and therefore, it is recommended only for emergency cases. Improvements in the chimney procedure may take place if the bypass grafts were larger (e.g. 10 mm diameter instead of 8 mm as in the model) and the stumps were shorter or eliminated. The length of the chimney graft should be as short as possible while ensuring graft fixation. The bypass between the LCCA and the LSA should be in the direction of flow as much as possible to reduce the risk of anastomosis failure. The results presented here may shade light on the hemodynamic factors and risk for complications, and provide insight into ways to improve the procedures. In addition, these results may imply that, when approved for clinical use, modular or fenestrated stent grafts designated for the aortic arch may improve the outcomes of endograft procedures in use nowadays.
Conflict of Interest We have no conflict of interest to disclose.
Acknowledgments We wish to thank Ms. Melanie Ratan and Ms. Shirly Steinlauf for their assistance.
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References Al Kindi, A.H., Al Kimyani, N., Alameddine, T., Al Abri, Q., Balan, B., Al Sabti, H., 2014. “Open” approach to aortic arch aneurysm repair. J. Saudi Heart Assoc. 26 (3), 152–161. Antoniou, G., El Sakka, K., Hamady, M., Wolfe, J., 2010. Hybrid treatment of complex aortic arch disease with supra-aortic debranching and endovascular stent graft repair. Eur. J. Vasc. Endovasc. Surg. 39 (6), 683–690. Avrahami, I., 2013. A finite element CFD simulation for predicting patient-specific hemodynamics of an aortic coarctation. International Workshop on Statistical Atlases and Computational Models of the Heart, Springer. Avrahami, I., Brand, M., Meirson, T., OvadiaBlechman, Z., Halak, M., 2012. Hemodynamic and mechanical aspects of fenestrated endografts for treatment of abdominal aortic aneurysm. Eur. J.Mech. B. Fluids 35, 85–91. Avrahami, I., Dilmoney, B., Azuri, A., Brand, M., Cohen, O., Shani, L., Nir, R.R., Bolotin, 2013. Investigation of risks for cerebral embolism associated with the hemodynamics of cardiopulmonary bypass cannula: a numerical model. Artif. Organs 37 (10), 857–865. Baldwin, Z.K., Chuter, T.A., Hiramoto, J.S., Reilly, L.M., Schneider, D.B., 2008. Doublebarrel technique for endovascular exclusion of an aortic arch aneurysm without sternotomy. J. Endovasc. Ther. 15 (2), 161–165. Bavaria, J., Vallabhajosyula, P., Moeller, P., Szeto, W., Desai, N., Pochettino, A., 2013. Hybrid approaches in the treatment of aortic arch aneurysms: postoperative and midterm outcomes. J. Thorac. Cardiovasc. Surg. 145 (3, Supplement), S85–S90. Benrashid, E., Wang, H., Keenan, J.E., Andersen, N.D., Meza, J.M., McCann, R.L., Hughes, G.C., 2016. Evolving practice pattern changes and outcomes in the era of hybrid aortic arch repair. J. Vasc. Surg. 63 (2), 323–331 (e321). Borghi, A., Wood, N.B., Mohiaddin, R.H., Xu, X.Y., 2008. Fluid–solid interaction simulation of flow and stress pattern in thoracoabdominal aneurysms: a patient-specific study. J. Fluids Struct. 24 (2), 270–280. Brand, M., Avrahami, I., Nardi, A., Silverberg, D., Halak, M., 2013 "Clinical, Hemodynamics and Mechanical Aspects of Aortic Aneurisms and Endovascular Repair" in "Aortic Aneurysms: Risk Factors, Diagnosis, Surgery & Repair." ED. Kuivaniemi, H., et al.: Nova Publisher, 181-192. Brinkman, W.T., Szeto, W.Y., Bavaria, J.E., 2007. Stent graft treatment for transverse arch and descending thoracic aorta aneurysms. Curr. Opin. Cardiol. 22 (6), 510. Buth, J., Penn, O., Tielbeek, A., Mersman, M., 1998. Combined approach to stentgraft treatment of an aortic arch aneurysm. J. Endovasc. Ther. 5 (4), 329–332. Canstein, C., Cachot, P., Faust, A., Stalder, A., Bock, J., Frydrychowicz, A., Küffer, J., Hennig, J., Markl, M., 2008. 3D MR flow analysis in realistic rapid‐prototyping model systems of the thoracic aorta: comparison with in vivo data and computational fluid dynamics in identical vessel geometries. Magn. Reson. Med. 59 (3), 535–546. Chuter, T.A.M., Schneider, D.B., Reilly, L.M., Lobo, E.P., Messina, L.M., 2003. Modular branched stent graft for endovascular repair of aortic arch aneurysm and dissection. J. Vasc. Surg. 38 (4), 859–863. Cires, G., Noll, R.E., Albuquerque, F.C., Tonnessen, B.H., Sternbergh, W.C., 2011. Endovascular debranching of the aortic arch during thoracic endograft repair. J. Vasc. Surg. 53 (6), 1485–1491. Criado, F.J., Clark, N.S., Barnatan, M.F., 2002. Stent graft repair in the aortic arch and descending thoracic aorta: a 4-year experience. J. Vasc. Surg. 36 (6), 1121–1128. Crosetto, P., Reymond, P., Deparis, S., Kontaxakis, D., Stergiopulos, N., Quarteroni, A., 2011. Fluid–structure interaction simulation of aortic blood flow. Comput. Fluids 43 (1), 46–57. Currens, J.H., 1948. A comparison of the blood pressure in the lying and standing positions: a study of five hundred men and five hundred women. Am. heart J. 35 (4), 646–654. Davies, P.F., 2009. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc Med 6 (1), 16–26. Dawson, E.A., Secher, N.H., Dalsgaard, M.K., Ogoh, S., Yoshiga, C.C., Gonzalez-Alonso, J., Steensberg, A., Raven, P.B., 2004. Standing up to the challenge of standing: a siphon does not support cerebral blood flow in humans. Am. J. Physiol.-Regul., Integr. Comp. Physiol. 287 (4), R911–R914. Di Martino, E.S., Guadagni, G., Fumero, A., Ballerini, G., Spirito, R., Biglioli, P., Redaelli, A., 2001. Fluid-structure interaction within realistic three-dimensional models of the aneurysmatic aorta as a guidance to assess the risk of rupture of the aneurysm. Med Eng. Phys. 23 (9), 647–655. Einav, S., Bluestein, D., 2004. Dynamics of blood flow and platelet transport in pathological vessels. Card. Eng.: Genes Cells Struct. Funct. 1015, 351–366. Feliciani, G., Potters, W.V., van Ooij, P., Schneiders, J.J., Nederveen, A.J., van Bavel, E., Majoie, C.B., Marquering, H.A., 2015. Multiscale 3-D þ t intracranial aneurysmal flow vortex detection. IEEE Trans. Biomed. Eng. 62 (5), 1355–1362. Figueroa, C.A., Taylor, C.A., Chiou, A.J., Yeh, V., Zarins, C.K., 2009. Magnitude and direction of pulsatile displacement forces acting on thoracic aortic endografts. J. Endovasc. Ther. 16 (3), 350–358. Fung, Y.C. Biomechanics: mechanical properties of living tissues. Springer Science & Business Media, 2013. Geisbüsch, P., Kotelis, D., Müller–Eschner, M., Hyhlik-Dürr, A., Böckler, D., 2011. Complications after aortic arch hybrid repair. J. Vasc. Surg. 53 (4), 935–941. Gottardi, R., Seitelberger, R., Zimpfer, D., Lammer, J., Wolner, E., Grimm, M., Czerny, M., 2005. An alternative approach in treating an aortic arch aneurysm with an anatomic variant by supraaortic reconstruction and stent-graft placement. J. Vasc. Surg. 42 (2), 357–360.
Hager, A., Kaemmerer, H., Rapp-Bernhardt, U., Blücher, S., Rapp, K., Bernhardt, T.M., Galanski, M., Hess, J., 2002. Diameters of the thoracic aorta throughout life as measured with helical computed tomography. J. Thorac. Cardiovasc. Surg. 123 (6), 1060–1066. Hill, L., 1895. The influence of the force of gravity on the circulation of the blood. J. Physiol. 18 (1-2), 15–53. Hugo, G.B., Michael, H.B., 1994. Blood flow measurements in the aorta and major arteries with MR velocity mapping. J. Magn. Reson. Imaging 4 (2), 119–130. Ishimaru, S., 2004. Endografting of the aortic arch. J. Endovasc. Ther. 11 (SupplementII), 62–71. Jakanani, G., Adair, W., 2010. Frequency of variations in aortic arch anatomy depicted on multidetector CT. Clin. Radiol. 65 (6), 481–487. Jin, S., Oshinski, J., Giddens, D.P., 2003. Effects of wall motion and compliance on flow patterns in the ascending aorta. J. Biomech. Eng. 125 (3), 347–354. Kawatani, Y., Hayashi, Y., Ito, Y., Kurobe, H., Nakamura, Y., Suda, Y., Hori, T., 2015. A case of ruptured aortic arch aneurysm successfully treated by thoracic endovascular aneurysm repair with chimney graft. Case Rep. Surg. 2015. Khanafer, K.M., Bull, J.L., Berguer, R., 2009. Fluid-structure interaction of turbulent pulsatile flow within a flexible wall axisymmetric aortic aneurysm model. Eur. J. Mech. - B/Fluids 28 (1), 88–102. Konoura, C., Yagi, T., Nakamura, M., Iwasaki, K., Qian, Y., Okuda, S., Yoshitake, A., Shimizu, H., Yozu, R., Umezu, M., 2013. Numerical analysis of blood flow distribution in 4- and 3-branch vascular grafts. J. Artif. Organs 16 (2), 157–163. Lam, S.K., Fung, G.S.K., Cheng, S.W.K., Chow, K.W., 2008. A computational study on the biomechanical factors related to stent-graft models in the thoracic aorta. Med. Biol. Eng. Comput. 46 (11), 1129–1138. Lantz, J., Ebbers, T., Engvall, J., Karlsson, M., 2013. Numerical and experimental assessment of turbulent kinetic energy in an aortic coarctation. J. Biomech. 46 (11), 1851–1858. Linnarsson, D., Sundberg, C., Tedner, B., Haruna, Y., Karemaker, J., Antonutto, G., Di Prampero, P., 1996. Blood pressure and heart rate responses to sudden changes of gravity during exercise. Am. J. Physiol.-Heart Circ. Physiol. 270 (6), H2132–H2142. Liu, K.-S., Lee, C.-H., Tsai, F.-C., Jhong, G.-H., Hung, K.-C., Liu, S.-J., 2015. Computational analysis of the mechanical behaviors of hemiarch and total arch replacements. Ann. Biomed. Eng. 43 (12), 2881–2891. Liu, X., Fan, Y., Deng, X., Zhan, F., 2011. Effect of non-Newtonian and pulsatile blood flow on mass transport in the human aorta. J. Biomech. 44 (6), 1123–1131. Liu, X., Pu, F., Fan, Y., Deng, X., Li, D., Li, S., 2009a. 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. Am. J. Physiol. - Heart Circ. Physiol. 297 (1), H163–H170. Liu, X., Pu, F., Fan, Y., Deng, X., Li, D., Li, S., 2009b. 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. Am. J. Physiol.-Heart Circ. Physiol. 297 (1), H163. Makaroun, M.S., Dillavou, E.D., Wheatley, G.H., Cambria, R.P., Investigators, G.T., 2008. Five-year results of endovascular treatment with the Gore TAG device compared with open repair of thoracic aortic aneurysms. J. Vasc. Surg. 47 (5), 912–918. Markl, M., Wagner, G.J., Barker, A.J., 2016. Re: blood flow analysis of the aortic arch using computational fluid dynamics, Eur. J. Cardio-Thoracic Surg., pp. 1586–1587, ezv480. Martin, G., Riga, C., Gibbs, R., Jenkins, M., Hamady, M., Bicknell, C., 2016. Short- and long-term results of hybrid arch and proximal descending thoracic aortic repair: a benchmark for new technologies.". J. Endovasc. Ther. 23 (5), 783–790. Melissano, G., Civilini, E., Bertoglio, L., Calliari, F., Setacci, F., Calori, G., Chiesa, R., 2007. Results of endografting of the aortic arch in different landing zones. Eur. J. Vasc. Endovasc. Surg. 33 (5), 561–566. Midulla, M., Moreno, R., Baali, A., Chau, M., Negre-Salvayre, A., Nicoud, F., Pruvo, J.P., Haulon, S., Rousseau, H., 2012. Haemodynamic imaging of thoracic stentgrafts by computational fluid dynamics (CFD): presentation of a patient-specific method combining magnetic resonance imaging and numerical simulations. Eur. Radiol. 22 (10), 2094–2102. Milewski, R.K., Szeto, W.Y., Pochettino, A., Moser, G.W., Moeller, P., Bavaria, J.E., 2010. Have hybrid procedures replaced open aortic arch reconstruction in highrisk patients? A comparative study of elective open arch debranching with endovascular stent graft placement and conventional elective open total and distal aortic arch reconstruction. J. Thorac. Cardiovasc. Surg. 140 (3), 590–597. Morris, L., Delassus, P., Callanan, A., Walsh, M., Wallis, F., Grace, P., McGloughlin, T., 2005. 3-D numerical simulation of blood flow through models of the human aorta. J. Biomech. Eng. 127, 767. Moulakakis, K.G., Mylonas, S.N., Dalainas, I., Sfyroeras, G.S., Markatis, F., Kotsis, T., Kakisis, J., Liapis, C.D., 2013. The chimney-graft technique for preserving supraaortic branches: a review. Ann. Cardiothorac. Surg. 2 (3), 339–346. Naughton, P.A., Park, M.S., Morasch, M.D., Rodriguez, H.E., Garcia-Toca, M., Wang, C. E., Eskandari, M.K., 2012. Emergent repair of acute thoracic aortic catastrophes: a comparative analysis. Arch. Surg. 147 (3), 243–249. Nauta, F.J.H., Conti, M., Kamman, A.V., van Bogerijen, G.H.W., Tolenaar, J.L., Auricchio, F., Figueroa, C.A., van Herwaarden, J.A., Moll, F.L., Trimarchi, S., 2015. Biomechanical changes after thoracic endovascular aortic repair in type B dissection: a systematic review. J. Endovasc. Ther. 22 (6), 918–933. Ohrlander, T., Sonesson, B., Ivancev, K., Resch, T., Dias, N., Malina, M., 2008. The chimney graft: a technique for preserving or rescuing aortic branch vessels in stent-graft sealing zones. J. Endovasc. Ther. 15 (4), 427–432.
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Patel, H.J., Deeb, G.M., 2008. Ascending and arch aorta pathology, natural history, and treatment. Circulation 118 (2), 188–195. Reneman, R.S., Arts, T., Hoeks, A.P., 2006. Wall shear stress–an important determinant of endothelial cell function and structure–in the arterial system in vivo. J. Vasc. Res. 43 (3), 251–269. Rissland, P., Alemu, Y., Einav, S., Ricotta, J., Bluestein, D., 2009. Abdominal aortic aneurysm risk of rupture: patient-specific FSI simulations using anisotropic model. J. Biomech. Eng. 131, 031001. Saleh, H.M., Inglese, L., 2006. Combined surgical and endovascular treatment of aortic arch aneurysms. J. Vasc. Surg. 44 (3), 460–466 (e461). Shahcheraghi, N., Dwyer, H.A., Cheer, A.Y., Barakat, A.I., Rutaganira, T., 2002. Unsteady and three-dimensional simulation of blood flow in the human aortic arch. J. Biomech. Eng. 124, 378. Shirakawa, Y., Kuratani, T., Shimamura, K., Torikai, K., Sakamoto, T., Shijo, T., Sawa, Y., 2015. The efficacy and short-term results of hybrid thoracic endovascular repair into the ascending aorta for aortic arch pathologies. Eur. J. Cardio-Thorac. Surg. 43 (3), 1–11. Shrestha, M., Bachet, J., Bavaria, J., Carrel, T.P., Paulis, R. De, Bartolomeo, R. Di, Etz, C. D., Grabenwöger, M., Grimm, M., Haverich, A., 2015. Current status and recommendations for use of the frozen elephant trunk technique: a position paper by the Vascular Domain of EACTS. Eur. J. Cardio-Thorac. Surg. (ezv085) Sonesson, B., Resch, T., Allers, M., Malina, M., 2009. Endovascular total aortic arch replacement by in situ stent graft fenestration technique. J. Vasc. Surg. 49 (6), 1589–1591. Sotiropoulos, F., 2015. Fluid mechanics of heart valves and their replacements. Annu. Rev. Fluid Mech. 48 (1). Steinman, D.A., Vorp, D.A., Ethier, C.R., 2003. Computational modeling of arterial biomechanics: insights into pathogenesis and treatment of vascular disease. J. Vasc. Surg. 37 (5), 1118–1128. Stone, D.H., Brewster, D.C., Kwolek, C.J., LaMuraglia, G.M., Conrad, M.F., Chung, T.K., Cambria, R.P., 2006. Stent-graft versus open-surgical repair of the thoracic aorta: mid-term results. J. Vasc. Surg. 44 (6), 1188–1197. Sugiura, K., Sonesson, B., Akesson, M., Björses, K., Holst, J., Malina, M., 2009. The applicability of chimney grafts in the aortic arch. J. Cardiovasc. Surg. 50 (4), 475–481. Szeto, W.Y., Bavaria, J.E., Bowen, F.W., Woo, E.Y., Fairman, R.M., Pochettino, A., 2007. The hybrid total arch repair: brachiocephalic bypass and concomitant endovascular aortic arch stent graft placement. J. Card. Surg. 22 (2), 97–102. Tan, F.P.P., Borghi, A., Mohiaddin, R.H., Wood, N.B., Thom, S., Xu, X.Y., 2009. Analysis of flow patterns in a patient-specific thoracic aortic aneurysm model. Comput. Struct. 87 (11–12), 680–690. Tarbell, J.M., Shi, Z.-D., Dunn, J., Jo, H., 2014. Fluid mechanics, arterial disease, and gene expression. Annu. Rev. Fluid Mech. 46, 591–614.
165
Tse, K.M., Chiu, P., Lee, H.P., Ho, P., 2011. Investigation of hemodynamics in the development of dissecting aneurysm within patient-specific dissecting aneurismal aortas using computational fluid dynamics (CFD) simulations. J. Biomech. 44 (5), 827–836. van Bogerijen, G.H.W., Auricchio, F., Conti, M., Lefieux, A., Reali, A., Veneziani, A., Tolenaar, J.L., Moll, F.L., Rampoldi, V., Trimarchi, S., 2014. Aortic hemodynamics after thoracic endovascular aortic repair, with particular attention to the birdbeak configuration. J. Endovasc. Ther. 21 (6), 791–802. van Prehn, J., Vincken, K.L., Muhs, B.E., Barwegen, G.K.W., Bartels, L.W., Prokop, M., Moll, F.L., Verhagen, H.J.M., 2007. Toward endografting of the ascending aorta: insight into dynamics using dynamic cine-CTA. J. Endovasc. Ther. 14 (4), 551–560. Vasava, P., Jalali, P., Dabagh, M., Kolari, P.J., 2012. Finite element modelling of pulsatile blood flow in idealized model of human aortic arch: study of hypotension and hypertension. Comput. Math. Methods Med. 2012. Wentzel, J.J., Corti, R., Fayad, Z.A., Wisdom, P., Macaluso, F., Winkelman, M.O., Fuster, V., Badimon, J.J., 2005. Does shear stress modulate both plaque progression and regression in the thoracic aorta?: human study using serial magnetic resonance imaging. J. Am. Coll. Cardiol. 45 (6), 846–854. Xenos, M., Bluestein, D., 2011. Biomechanical aspects of abdominal aortic aneurysm (AAA) and its risk of rupture: fluid structure interaction (FSI) studies. Biomech. Mechanobiol. Aneurysms, 181–220. Yang, J., Liu, Y., Duan, W., Yi, D., Yu, S., Ma, R., Ren, J., 2016. A feasibility study of total endovascular aortic arch replacement: from stent-graft design to preclinical testing. J. Thorac. Cardiovasc. Surg. 151 (4), 1203–1212. Yang, J., Xiong, J., Liu, X., Jia, X., Zhu, Y., Guo, W., 2012. Endovascular chimney technique of aortic arch pathologies: a systematic review. Ann. Vasc. Surg. 26 (7), 1014–1021. Yokoi, Y., Azuma, T., Yamazaki, K., 2013. Advantage of a precurved fenestrated endograft for aortic arch disease: simplified arch aneurysm treatment in Japan 2010 and 2011. J. Thorac. Cardiovasc. Surg. 145 (3, Supplement), S103–S109. Yoshida, R., Kolvenbach, R., Yoshida, W., Wassijew, S., Schwierz, E., Lin, F., 2011. Total endovascular debranching of the aortic arch. Eur. J. Vasc. Endovasc. Surg. 42 (5), 627–630. Zerwes, S., Leissner, G., Gosslau, Y., Jakob, R., Bruijnen, H.-K., Oertl, F., Woelfle, K., 2015. Clinical outcomes in hybrid repair procedures for pathologies involving the aortic arch. Vascular 23 (1), 9–16. Zhang, P., Liu, X., Sun, A., Fan, Y., Deng, X., 2015. Hemodynamic insight into overlapping bare-metal stents strategy in the treatment of aortic aneurysm. J. Biomech. 48 (10), 2041–2046. Ziganshin, B.A., Elefteriades, J.A., 2013. Deep hypothermic circulatory arrest. Ann. Cardiothorac. Surg. 2 (3), 303–315.