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Copyright © 2014 International Center for Artificial Organs and Transplantation and Wiley Periodicals, Inc.
Dispersive Aortic Cannulas Reduce Aortic Wall Shear Stress Affecting Atherosclerotic Plaque Embolization *†‡Alexander Assmann, §Fethi Gül, §Ali Cemal Benim, ¶Franz Joos, *Payam Akhyari, and *Artur Lichtenberg *Research Group for Experimental Surgery and Department of Cardiovascular Surgery, Medical Faculty, Heinrich Heine University; §Computational Fluid Dynamics Lab, Department of Mechanical and Process Engineering, Düsseldorf University of Applied Sciences, Düsseldorf; ¶Laboratory of Turbomachinery, Helmut Schmidt University, Hamburg, Germany; †Department of Medicine, Center for Biomedical Engineering, Brigham and Women’s Hospital, Harvard Medical School, Boston; and ‡Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA, USA
Abstract: Neurologic complications during on-pump cardiovascular surgery are often induced by mobilization of atherosclerotic plaques, which is directly related to enhanced wall shear stress. In the present study, we numerically evaluated the impact of dispersive aortic cannulas on aortic blood flow characteristics, with special regard to the resulting wall shear stress profiles. An idealized numerical model of the human aorta and its branches was created and used to model straight as well as bent dispersive aortic cannulas with meshlike tips inserted in the distal ascending aorta. Standard cannulas with straight beveled or bent tips served as controls. Using a recently optimized computing method, simulations of pulsatile and nonpulsatile extracorporeal circulation were performed. Dispersive aortic cannulas reduced the maximum and
average aortic wall shear stress values to approximately 50% of those with control cannulas, while the difference in local values was even larger. Moreover, under pulsatile circulation, dispersive cannulas shortened the time period during which wall shear stress values were increased. The turbulent kinetic energy was also diminished by utilizing dispersive cannulas, reducing the risk of hemolysis. In summary, dispersive aortic cannulas decrease aortic wall shear stress and turbulence during extracorporeal circulation and may therefore reduce the risk of endothelial and blood cell damage as well as that of neurologic complications caused by atherosclerotic plaque mobilization. Key Words: Aortic blood flow—Aortic cannula— Extracorporeal circulation—Computational fluid dynamics—Wall shear stress—Plaque embolization.
One of the major adverse events that may occur during extracorporeal circulation (ECC) in cardiac surgery is arterial embolization of atherosclerotic plaques resulting in stroke or ischemia of other organs such as kidney, liver, or intestine. Besides being manually mobilized during cross-clamping of the aorta, plaques may delaminate or rupture due to the jet stream of the aortic inlet cannula of the heart– lung machine. This sandblastlike effect not only negatively affects atherosclerotic plaques but also
damages healthy endothelium in the area in which the cannula jet hits the aortic wall (1). Enhanced maximum wall shear stress (WSS) values have been reported to be correlated with the rupture of atherosclerotic plaques (2,3). Recently, our group has developed and validated a numerical model for simulating different ECC conditions in human aortic geometries (4,5). Using this model, it has been shown that nonpulsatile ECC remarkably reduces maximum WSS values as compared with pulsatile ECC. Previous simulation studies have underlined the importance of the cannulation site with regard to changes in the aortic blood flow profile (6,7). Another important component influencing the ECC-generated blood flow in the aorta is the tip shape of the arterial cannula. In experimental in vitro settings, different tip geometries have been tested,
doi:10.1111/aor.12359 Received March 2014; revised April 2014. Address correspondence and reprint requests to Dr. Alexander Assmann, Department of Cardiovascular Surgery, Medical Faculty, Heinrich Heine University, Moorenstr. 5, D–40225 Düsseldorf, Germany. E-mail: [email protected]
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focusing on the improvement of pressure gradients and back-pressure values (8,9). The present study aims at examining the effects of dispersive cannula tips on the aortic WSS profile under pulsatile and nonpulsatile ECC conditions. In order to obtain spatial and temporal WSS values for the whole human aorta, our recently validated numerical model for ECC simulations was applied. MATERIALS AND METHODS Aortic grid generation As the basis for all blood flow simulations, a numerical model of an idealized human aorta and its branches was created (Fig. 1A). Geometric data were imported into the grid generator Gambit (ANSYS, Canonsburg, PA, USA) and afterward transferred into the computational fluid dynamics modeling software Fluent (ANSYS). On the basis of grid independency studies in idealized geometries (5), a mesh structure was generated, consisting of approximately 700 000 tetrahedral and hexahedral elements (Fig. 1B). The assessment of grid independency was based not only on the velocity field but also on the WSS.
FIG. 1. Numerically modeled mesh of an idealized human aorta and its branches (A,B) with inserted dispersive (C) or standard (D) ECC cannulas (versions with bent tips are displayed to show the different lead-in angles of 80° or 90° for bent cannulas as a consequence of their geometry). A, cannula inlet; B, brachiocephalic trunk; C, left common carotid artery; D, left subclavian artery; E, celiac trunk; F, superior mesenteric artery; G, left renal artery; H, right renal artery; I, left common iliac artery; K, right common iliac artery. Artif Organs, Vol. 39, No. 3, 2015
On the level of the ascending aorta, vascular crossclamping was assumed, simulating the situation during ECC with cardiac arrest. Straight as well as bent dispersive aortic cannulas (Sorin Optiflow, Sorin, Milan, Italy) were compared with each other and with straight as well as bent standard end-hole cannulas. The insertion site was the distal ascending aorta, cannulated with a lead-in angle of 80° for the bent dispersive cannula or 90° for the bent standard cannula (Fig. 1C,D). The center of each cannula tip was positioned in the center of the vessel lumen. Mathematical and numerical formulation The mathematical/numerical model for simulating ECC in aortic geometries has been recently validated and published by the authors (4). Three-dimensional steady-state or pulsatile flow was analyzed. The aortic wall distensibility was neglected. Shear stresses in large arteries are typically sufficiently large to assume that blood behaves as a Newtonian fluid (10). Thus, Navier–Stokes equations were solved with constant material properties. Reynolds numbers (Re) larger than around 2000 (Re is based on bulk flow velocity and local channel diameter) indicate transition from laminar to turbulent flow. As the peak or even time-averaged inlet Re values occurring in cannula perfusion exceed this value by far, flow turbulences need to be considered for an adequate turbulence model. On the other hand, due to temporarily low inlet velocities during pulsatile perfusion, very low Re values also occur. Thus, the turbulence model should allow for transitional turbulence, too. In the present study, the turbulence/viscosity-based two-equation “shear stress transport” turbulence model was applied, which had been observed in a previous study (11) to generally accommodate such effects. The governing equations were discretized by a colocated finitevolume method (12). With regard to the velocity– pressure coupling, the SIMPLEC algorithm was used for steady-state computations (13) and the PISO algorithm for pulsatile flow (14). Power law was utilized for discretization of the convective terms (12). Blood flow simulations Simulations were conducted of antegrade blood flow via dispersive or standard cannulas with straight or bent tips inserted in the distal ascending aorta. Moreover, physiological flow originating from the proximal ascending aorta was computed as control. For each ECC setting, pulsatile and nonpulsatile blood flow were considered, whereas the pulse waveform mimicked the physiological pulse, as recently published (4). The flow rate was set to 4 L/min
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FIG. 2. Cannula outlet flow profiles for different tip shapes: A, straight dispersive cannula; B, straight end-hole cannula; C, bent dispersive cannula; D, bent end-hole cannula.
(cardiac index 2.4 L/min/m2), assuming a mean arterial blood pressure of 13 kPa and a mean central venous pressure of 1 kPa. The spatial flow distribution at the inlet relied on bulk profiles. The aortic outlet boundary conditions were defined by loss coefficients, as recently reported by the authors (4,5). Whole aortic profiles for WSS and turbulent kinetic energy (TKE) were derived from the blood flow computations. RESULTS The profile of the blood flow at the cannula outlets is displayed in Fig. 2 for all cannula tip settings, indi-
cating the dispersive properties of the meshlike tips. Table 1 shows that for all ECC settings, the distribution of the blood flow to the aortic branches was similar to physiological flow conditions. In order to comparatively examine the sandblasting effect of different cannula tip shapes, aortic WSS profiles were analyzed for each ECC setting. In general, the highest WSS values occurred in the area around the spot at which the cannula jet stream hit the aortic wall. In the case of straight cannulas, the primarily affected area was the posterior wall of the ascending aorta, while bent cannulas directed the outflow jet toward the orifice of the brachiocephalic
TABLE 1. Distribution of blood flow (%) among the aortic branches by ECC setting Aortic branch B C D E F G H I K
Straight dispersive
Straight end-hole
Bent dispersive
Bent end-hole
Physiological flow
15.70 7.85 7.85 16.02 10.67 10.68 10.68 10.27 10.27
15.64 7.83 7.81 16.00 10.66 10.66 10.66 10.36 10.36
15.81 7.90 7.87 16.11 10.74 10.39 10.39 10.39 10.39
16.12 7.91 7.86 15.59 10.39 10.77 10.78 10.29 10.29
15.80 7.90 7.90 15.80 10.53 10.53 10.53 10.53 10.53
B, brachiocephalic trunk; C, left common carotid artery; D, left subclavian artery; E, celiac trunk; F, superior mesenteric artery; G, left renal artery; H, right renal artery; I, left common iliac artery; K, right common iliac artery. Artif Organs, Vol. 39, No. 3, 2015
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FIG. 3. WSS profiles resulting from nonpulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C), and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. WSS given in pascals.
trunk. Dispersive cannula tips remarkably reduced the area of enhanced WSS as compared with controls, whereas bent tips further diminished the stressed region. These observations applied to simulations of nonpulsatile (Fig. 3) as well as pulsatile (Figs. 4 and 5) ECC. For bent and straight tip shapes, dispersive geometries reduced not only the spatial extent but also the absolute amount of WSS exerted on the aortic walls: The maximum values for nonpulsatile ECC as well as for the average and peak WSS during pulsatile ECC were diminished by approximately 50% (Table 2). Moreover, dispersive cannulas shortened the time period of enhanced WSS in each cardiac cycle of pulsatile simulations. Enhanced TKE was observed in the same areas as increased WSS. The spatial extent as well as the maximum values of increased TKE were reduced by dispersive cannulas under pulsatile and nonpulsatile conditions (Fig. 6; Table 3). DISCUSSION In order to examine the influence of dispersive arterial cannula tips on the local aortic WSS profiles, a recently validated numerical approach for simulating the effect of ECC on the human aortic blood flow was applied (4,5). For pulsatile and nonpulsatile ECC, straight as well as bent dispersive tips were Artif Organs, Vol. 39, No. 3, 2015
shown to reduce the spatial and temporal extent as well as the maximum values of local WSS in the cannulated aorta, as compared with control cannulas with end-hole tips. Endothelial and blood cell damage ECC is a mandatory tool for many operative techniques in cardiac surgery, including proximal aortic surgery, heart transplantation, heart valve repair, and conventional replacement. For patients with coronary artery disease, off-pump coronary artery bypass grafting (OPCAB) is an epidemiologically important approach to avoiding ECC during coronary surgery. Although recent clinical trials have suggested a benefit of OPCAB regarding intraoperative stroke, the long-term outcome including mortality and myocardial infarction was not improved as compared with bypass surgery under ECC (15–18). Therefore, ECC remains an indispensable standard technique in cardiac surgery, and intensified research on decreasing the risk of ECC-associated complications is warranted. Arterial embolization of atherosclerotic plaques is a common event during ECC and frequently results in severe complications, such as stroke or ischemia of other organs such as kidney, liver, or intestine. The sandblastlike effect of conventional arterial ECC cannulas is a major risk factor of endothelial damage
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FIG. 4. Average WSS profiles resulting from pulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C), and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. WSS given in pascals.
and plaque mobilization. Enhanced arterial WSS caused by the cannula jet stream is known to induce endothelial damage. After 120-min cardiopulmonary bypass in a porcine model, endothelial lesions in primarily healthy intima have been reported (1). While
chronic increase of WSS seems to prevent the development of atherosclerotic plaques, high values have been observed to be colocalized with unstable or ruptured plaques (2,3,19). Intraoperative stroke is one of the major adverse consequences of plaque
FIG. 5. Maximum WSS profiles resulting from pulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C), and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. WSS given in pascals.
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A. ASSMANN ET AL. TABLE 2. Maximum values of aortic WSS by shape of the aortic cannula tip WSS (Pa) Cannula tip shape
Nonpulsatile perfusion*
Pulsatile perfusion†
Straight dispersive Straight end-hole Bent dispersive Bent end-hole
22 37 16 34
20/110 40/250 23/132 43/227
* Mean values. † Mean values/peak values.
delamination. As up to 10% of all cardiosurgical patients, and up to 16% in high-risk groups, exhibit neurological complications after ECC, the prevention of plaque embolization is of major interest not only with regard to the individual patient but also due to economic aspects (20). With the aim of reducing the sandblasting effect of conventional end-hole-tip cannulas, different cannula geometries have been developed. Jet stream dispersion has been achieved by dispersive meshlike and funnel-shaped tips as well as by spininducing stators in the main bodies of arterial ECC cannulas. In mock circulation experiments, these cannulas have been shown to provide lower pressure gradients, back-pressure values, and strain-rate tensors than conventional end-hole-tip cannulas (8,9,21,22). Recently, a numerical study on cannulas with diffuser-cone tips resulted in improved WSS conditions in the aortic arch as compared to endhole tips (23). Numerical analysis of a similar dif-
fuser cannula geometry additionally pointed to reduced risk of hemolysis (24). Our present study shows the hemodynamic superiority of straight as well as bent cannulas with dispersive meshlike tips. A major advantage of this approach over recently published designs is that the tip of the cannula is pointed, while the recently reported diffuser cannulas exhibit divergent walls at the tip. Practical application, that is, insertion of such cannulas with divergent walls into arteries, has to be regarded as very critical, as at the end of the insertion process, the diameter of the hole that has to be created in the artery in order to introduce the broad tip will be larger than the diameter of the cannula at the level of the artery wall. This will subsequently result in arterial bleeding from the insertion site. In contrast, the pointed-tipped cannula used in the present study occludes the insertion hole in the arterial wall, thus preventing bleeding from the insertion site, as is known from clinical application of this cannula.
FIG. 6. Maximum TKE profiles resulting from pulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C). and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. TKE given in m2/s2.
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DISPERSIVE AORTIC CANNULAS REDUCE SHEAR TABLE 3. Maximum values of aortic TKE during pulsatile perfusion by shape of aortic cannula tip Cannula tip shape
TKE (m2/s2)
Straight dispersive Straight end-hole Bent dispersive Bent end-hole
0.408 0.992 0.362 0.780
The validity of the present computations was improved by applying a recently developed numerical model of ECC simulations based on loss coefficients as aortic boundary conditions (5). In a previous study, we had shown a remarkable decrease of WSS during nonpulsatile ECC as compared with pulsatile perfusion (4). The present data confirm this observation and reveal the independent WSS-lowering effect of dispersive cannulas under pulsatile as well as nonpulsatile ECC conditions. In both ECC scenarios, the maximum values of average WSS resulting from dispersive cannula perfusion were similar to the maximum values under physiological blood flow obtained in our previous study. The best hemodynamic performance regarding potential endothelial damage was observed when simulating bent dispersive tips, although, due to the geometry of the cannula with its flat body–tip angle, the resulting blood flow at the cannula outlet was not directed parallel to the aorta, and thus, it hit the aortic wall very close to the outlet, leaving room for further improvement of the cannula design. In contrast, the end-hole control cannula was placed in an ideal position in the center of the aortic lumen, generating a jet stream more parallel to the aortic walls. As a consequence, the distance between the cannula outlet and the site at which the jet stream hit the aortic wall was larger for the control cannula, which may have diminished the WSS exerted on the aorta as compared with the dispersive cannula, for which there was a very short distance between outlet and impact site on the aortic wall. That the dispersive cannula showed better performance in spite of the less beneficial outlet orientation and outlet–wall distance suggests that the level of WSS evoked by dispersive cannulas is not sensitive to displacement of the cannula. This aspect is of actual clinical relevance, as even in the case of thorough initial cannula positioning, at least slight displacement of the cannula frequently occurs during the operation. The reduction of WSS by dispersive cannulas is all the more noteworthy, as the primarily affected areas are the posterior wall of the ascending aorta (in the case of straight cannulas) and the orifice of the brachiocephalic trunk (in the case of bent cannulas). Both regions exhibit a high prevalence of plaque for-
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mation in atherosclerotic patients (25,26). Therefore, decreasing the local WSS during ECC might have high clinical impact. Besides WSS, the extent of TKE was also diminished by utilizing dispersive cannulas. As turbulent flow is known to increase blood cell damage (27), dispersive meshlike tips might be preferable not only to prevent endothelial damage and plaque embolization but also in terms of hemolysis during ECC. In addition, more uniform flow distribution originating from dispersive cannulas might beneficially affect organ perfusion. In a previous study, it was shown that owing to the Venturi effect, the jet stream of a regular end-hole cannula can severely impede the flow to the aortic branches (6). Dispersion of the cannula stream may reduce this effect, increase the pressure in the near field of the stream, and thus prevent malperfusion of branches that are located very close to the outlet of the cannula. Clinical data on the effect of aortic cannula design Despite the significance of reducing intraoperative plaque embolization during ECC, only a small number of clinical studies on the effect of aortic cannula design on ECC-associated complications exists so far. Weinstein et al. analyzed data from coronary artery bypass grafting (CABG) patients with intraoperative stroke and found predominantly lefthemispheric locations. As they could show that the utilized end-hole cannulas caused a high-velocity jet toward the orifice of the left common carotid artery, and aortic manipulation—for example by crossclamping, which is another possible risk factor of stroke—is believed to preferentially induce embolization into the contiguous brachiocephalic trunk, the investigators concluded that the cannula jet stream was a major reason for the occurrence of stroke (28). In 137 stroke patients after CABG, aortic cannulas with bent tips have been shown to significantly reduce the incidence as well as the severity of strokes as compared to straight cannulas (29). An echocardiographic study on the outlet flow profile of different aortic cannulas in humans revealed significantly reduced velocities for dispersive cannulas versus nondispersive models (30). A small case series evaluating diffuser-tip cannulas in CABG patients showed a diminished risk of cerebral gaseous and particle emboli when compared with previous data on standard end-hole cannulas (31). In summary, the existing literature suggests a beneficial effect of dispersive cannulas on the occurrence of intraoperative stroke during ECC. However, the clinical evidence is quite restricted, and randomized Artif Organs, Vol. 39, No. 3, 2015
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controlled trials examining the actual potential of dispersive aortic cannulas are warranted. Limitations of the study The distensibility of the physiological human aortic wall, which might influence blood flow profiles during pulsatile ECC, has not been considered in this study. However, the simulations are focused on patients with severe atherosclerosis, who account for the majority of cardiosurgical patients nowadays. Atherosclerotic and arteriosclerotic wall remodeling in the elderly leads to increased wall thickness and structural damage, both contributing to enhanced wall stiffness (32). In these patients, aortic wall distensibility is either lost or locally impaired in a heterogeneous pattern, which strongly impedes any attempt to simulate their individual profile of wall distensibility. As an idealized aortic geometry was utilized, the current approach allows for a general comparative examination of dispersive versus standard cannula tips. However, future MRI-supported animal ECC studies will have to reveal the effect of dispersive cannulas on the WSS profiles as well as on the resulting biological effect on the endothelium in individualized aortic geometries. CONCLUSIONS Based on our recently developed and validated numerical model for simulating the effect of extracorporeal circulation on human aortic blood flow, the present study shows that straight as well as bent arterial cannulas with meshlike dispersive tips improve aortic wall shear stress and turbulence profiles. Moreover, this effect was observed to be independent of whether pulsatile or nonpulsatile flow was applied. Thus, dispersive cannulas have the potential to reduce ECC-related complications such as stroke, endothelial damage, and hemolysis. Acknowledgments: The authors gratefully acknowledge Sorin Group (Milan, Italy) for financial support of this project. The study sponsor did not influence study design, collection, analysis or interpretation of data, writing of the manuscript, or the decision to submit the manuscript for publication. Conflict of Interest: None. REFERENCES 1. Schnürer C, Hager M, Györi G, et al. Evaluation of aortic cannula jet lesions in a porcine cardiopulmonary bypass (CPB) model. J Cardiovasc Surg 2011;52:105–9.
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2. Groen HC, Gijsen FJ, van der Lugt A, et al. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke 2007;38:2379–81. 3. Tang D, Teng Z, Canton G, et al. Sites of rupture in human atherosclerotic carotid plaques are associated with high structural stresses: an in vivo MRI-based 3D fluid-structure interaction study. Stroke 2009;40:3258–63. 4. Assmann A, Benim AC, Gül F, et al. Pulsatile extracorporeal circulation during on-pump cardiac surgery enhances aortic wall shear stress. J Biomech 2012;45:156–63. 5. Benim AC, Nahavandi A, Assmann A, Schubert D, Feindt P, Suh SH. Simulation of blood flow in human aorta with emphasis on outlet boundary conditions. Appl Math Model 2011;35:3175–88. 6. Kaufmann TA, Hormes M, Laumen M, et al. The impact of aortic/subclavian outflow cannulation for cardiopulmonary bypass and cardiac support: a computational fluid dynamics study. Artif Organs 2009;33:727–32. 7. Kaufmann TA, Hormes M, Laumen M, et al. Flow distribution during cardiopulmonary bypass in dependency on the outflow cannula positioning. Artif Organs 2009;33:988–92. 8. Scharfschwerdt M, Richter A, Boehmer K, Repenning D, Sievers HH. Improved hydrodynamics of a new aortic cannula with a novel tip design. Perfusion 2004;19:193–7. 9. White JK, Jagannath A, Titus J, Yoneyama R, Madsen J, Agnihotri AK. Funnel-tipped aortic cannula for reduction of atheroemboli. Ann Thorac Surg 2009;88:551–7. 10. Pedley TJ. Arterial and venous fluid dynamics. In: Pedrizzetti G, Perktold K, eds. Cardiovascular Fluid Mechanics. Vienna: Springer, 2003;73–136. 11. Benim AC, Pasqualotto E, Suh SH. Modeling turbulent flow past a circular cylinder by RANS, URANS, LES and DES. Prog Comput Fluid Dy 2008;8:299–307. 12. Versteeg HK, Malalasekera W. An Introduction to Computational Fluid Dynamics—The Finite Volume Method, 2nd Edition. Harlow, UK: Pearson Education, 2007. 13. Van Doormal JP, Raithby GD. Enhancements of the SIMPLE method for predicting incompressible fluid flows. Num Heat Transfer 1984;7:147–63. 14. Issa RI. Solution of the implicitly discretised fluid flow equations by operator-splitting. J Comput Phys 1986;62:40– 65. 15. Afilalo J, Rasti M, Ohayon SM, Shimony A, Eisenberg MJ. Off-pump vs. on-pump coronary artery bypass surgery: an updated meta-analysis and meta-regression of randomized trials. Eur Heart J 2012;33:1257–67. 16. Houlind K, Kjeldsen BJ, Madsen SN, et al. On-pump versus off-pump coronary artery bypass surgery in elderly patients: results from the Danish On-Pump versus Off-Pump Randomization Study. Circulation 2012;125:2431–9. 17. Marui A, Okabayashi H, Komiya T, et al. Benefits of off-pump coronary artery bypass grafting in high-risk patients. Circulation 2012;126:S151–7. 18. Puskas JD, Williams WH, O’Donnell R, et al. Off-pump and on-pump coronary artery bypass grafting are associated with similar graft patency, myocardial ischemia, and freedom from reintervention: long-term follow-up of a randomized trial. Ann Thorac Surg 2011;91:1836–42. 19. Tang D, Teng Z, Canton G, et al. Local critical stress correlates better than global maximum stress with plaque morphological features linked to atherosclerotic plaque vulnerability: an in vivo multi-patient study. Biomed Eng Online 2009;8: 15. 20. Wolman RL, Nussmeier NA, Aggarwal A, et al. Cerebral injury after cardiac surgery: identification of a group at extraordinary risk. Multicenter Study of Perioperative Ischemia Research Group (McSPI) and the Ischemia Research Education Foundation (IREF) Investigators. Stroke 1999;30:514–22. 21. Minakawa M, Fukuda I, Yamazaki J, Fukui K, Yanaoka H, Inamura T. Effect of cannula shape on aortic wall and flow
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28. Weinstein GS. Left hemispheric strokes in coronary surgery: implications for end-hole aortic cannulas. Ann Thorac Surg 2001;71:128–32. 29. Albert AA, Beller CJ, Arnrich B, et al. Is there any impact of the shape of aortic end-hole cannula on stroke occurrence? Clinical evaluation of straight and bent-tip aortic cannulae. Perfusion 2002;17:451–6. 30. Grooters RK, Ver Steeg DA, Stewart MJ, Thieman KC, Schneider RF. Echocardiographic comparison of the standard end-hole cannula, the soft-flow cannula, and the dispersion cannula during perfusion into the aortic arch. Ann Thorac Surg 2003;75:1919–23. 31. Lata AL, Hammon JW, Deal DD, Stump DA, Kincaid EH, Kon ND. Cannula design reduces particulate and gaseous emboli during cardiopulmonary bypass for coronary revascularization. Perfusion 2011;26:239–44. 32. Mitchell GF. Arterial stiffness and wave reflection: biomarkers of cardiovascular risk. Artery Res 2009;3:56– 64.
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Dispersive Aortic Cannulas Reduce Aortic Wall Shear Stress Affecting Atherosclerotic Plaque Embolization *†‡Alexander Assmann, §Fethi Gül, §Ali Cemal Benim, ¶Franz Joos, *Payam Akhyari, and *Artur Lichtenberg *Research Group for Experimental Surgery and Department of Cardiovascular Surgery, Medical Faculty, Heinrich Heine University; §Computational Fluid Dynamics Lab, Department of Mechanical and Process Engineering, Düsseldorf University of Applied Sciences, Düsseldorf; ¶Laboratory of Turbomachinery, Helmut Schmidt University, Hamburg, Germany; †Department of Medicine, Center for Biomedical Engineering, Brigham and Women’s Hospital, Harvard Medical School, Boston; and ‡Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA, USA
Abstract: Neurologic complications during on-pump cardiovascular surgery are often induced by mobilization of atherosclerotic plaques, which is directly related to enhanced wall shear stress. In the present study, we numerically evaluated the impact of dispersive aortic cannulas on aortic blood flow characteristics, with special regard to the resulting wall shear stress profiles. An idealized numerical model of the human aorta and its branches was created and used to model straight as well as bent dispersive aortic cannulas with meshlike tips inserted in the distal ascending aorta. Standard cannulas with straight beveled or bent tips served as controls. Using a recently optimized computing method, simulations of pulsatile and nonpulsatile extracorporeal circulation were performed. Dispersive aortic cannulas reduced the maximum and
average aortic wall shear stress values to approximately 50% of those with control cannulas, while the difference in local values was even larger. Moreover, under pulsatile circulation, dispersive cannulas shortened the time period during which wall shear stress values were increased. The turbulent kinetic energy was also diminished by utilizing dispersive cannulas, reducing the risk of hemolysis. In summary, dispersive aortic cannulas decrease aortic wall shear stress and turbulence during extracorporeal circulation and may therefore reduce the risk of endothelial and blood cell damage as well as that of neurologic complications caused by atherosclerotic plaque mobilization. Key Words: Aortic blood flow—Aortic cannula— Extracorporeal circulation—Computational fluid dynamics—Wall shear stress—Plaque embolization.
One of the major adverse events that may occur during extracorporeal circulation (ECC) in cardiac surgery is arterial embolization of atherosclerotic plaques resulting in stroke or ischemia of other organs such as kidney, liver, or intestine. Besides being manually mobilized during cross-clamping of the aorta, plaques may delaminate or rupture due to the jet stream of the aortic inlet cannula of the heart– lung machine. This sandblastlike effect not only negatively affects atherosclerotic plaques but also
damages healthy endothelium in the area in which the cannula jet hits the aortic wall (1). Enhanced maximum wall shear stress (WSS) values have been reported to be correlated with the rupture of atherosclerotic plaques (2,3). Recently, our group has developed and validated a numerical model for simulating different ECC conditions in human aortic geometries (4,5). Using this model, it has been shown that nonpulsatile ECC remarkably reduces maximum WSS values as compared with pulsatile ECC. Previous simulation studies have underlined the importance of the cannulation site with regard to changes in the aortic blood flow profile (6,7). Another important component influencing the ECC-generated blood flow in the aorta is the tip shape of the arterial cannula. In experimental in vitro settings, different tip geometries have been tested,
doi:10.1111/aor.12359 Received March 2014; revised April 2014. Address correspondence and reprint requests to Dr. Alexander Assmann, Department of Cardiovascular Surgery, Medical Faculty, Heinrich Heine University, Moorenstr. 5, D–40225 Düsseldorf, Germany. E-mail: [email protected]
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focusing on the improvement of pressure gradients and back-pressure values (8,9). The present study aims at examining the effects of dispersive cannula tips on the aortic WSS profile under pulsatile and nonpulsatile ECC conditions. In order to obtain spatial and temporal WSS values for the whole human aorta, our recently validated numerical model for ECC simulations was applied. MATERIALS AND METHODS Aortic grid generation As the basis for all blood flow simulations, a numerical model of an idealized human aorta and its branches was created (Fig. 1A). Geometric data were imported into the grid generator Gambit (ANSYS, Canonsburg, PA, USA) and afterward transferred into the computational fluid dynamics modeling software Fluent (ANSYS). On the basis of grid independency studies in idealized geometries (5), a mesh structure was generated, consisting of approximately 700 000 tetrahedral and hexahedral elements (Fig. 1B). The assessment of grid independency was based not only on the velocity field but also on the WSS.
FIG. 1. Numerically modeled mesh of an idealized human aorta and its branches (A,B) with inserted dispersive (C) or standard (D) ECC cannulas (versions with bent tips are displayed to show the different lead-in angles of 80° or 90° for bent cannulas as a consequence of their geometry). A, cannula inlet; B, brachiocephalic trunk; C, left common carotid artery; D, left subclavian artery; E, celiac trunk; F, superior mesenteric artery; G, left renal artery; H, right renal artery; I, left common iliac artery; K, right common iliac artery. Artif Organs, Vol. 39, No. 3, 2015
On the level of the ascending aorta, vascular crossclamping was assumed, simulating the situation during ECC with cardiac arrest. Straight as well as bent dispersive aortic cannulas (Sorin Optiflow, Sorin, Milan, Italy) were compared with each other and with straight as well as bent standard end-hole cannulas. The insertion site was the distal ascending aorta, cannulated with a lead-in angle of 80° for the bent dispersive cannula or 90° for the bent standard cannula (Fig. 1C,D). The center of each cannula tip was positioned in the center of the vessel lumen. Mathematical and numerical formulation The mathematical/numerical model for simulating ECC in aortic geometries has been recently validated and published by the authors (4). Three-dimensional steady-state or pulsatile flow was analyzed. The aortic wall distensibility was neglected. Shear stresses in large arteries are typically sufficiently large to assume that blood behaves as a Newtonian fluid (10). Thus, Navier–Stokes equations were solved with constant material properties. Reynolds numbers (Re) larger than around 2000 (Re is based on bulk flow velocity and local channel diameter) indicate transition from laminar to turbulent flow. As the peak or even time-averaged inlet Re values occurring in cannula perfusion exceed this value by far, flow turbulences need to be considered for an adequate turbulence model. On the other hand, due to temporarily low inlet velocities during pulsatile perfusion, very low Re values also occur. Thus, the turbulence model should allow for transitional turbulence, too. In the present study, the turbulence/viscosity-based two-equation “shear stress transport” turbulence model was applied, which had been observed in a previous study (11) to generally accommodate such effects. The governing equations were discretized by a colocated finitevolume method (12). With regard to the velocity– pressure coupling, the SIMPLEC algorithm was used for steady-state computations (13) and the PISO algorithm for pulsatile flow (14). Power law was utilized for discretization of the convective terms (12). Blood flow simulations Simulations were conducted of antegrade blood flow via dispersive or standard cannulas with straight or bent tips inserted in the distal ascending aorta. Moreover, physiological flow originating from the proximal ascending aorta was computed as control. For each ECC setting, pulsatile and nonpulsatile blood flow were considered, whereas the pulse waveform mimicked the physiological pulse, as recently published (4). The flow rate was set to 4 L/min
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FIG. 2. Cannula outlet flow profiles for different tip shapes: A, straight dispersive cannula; B, straight end-hole cannula; C, bent dispersive cannula; D, bent end-hole cannula.
(cardiac index 2.4 L/min/m2), assuming a mean arterial blood pressure of 13 kPa and a mean central venous pressure of 1 kPa. The spatial flow distribution at the inlet relied on bulk profiles. The aortic outlet boundary conditions were defined by loss coefficients, as recently reported by the authors (4,5). Whole aortic profiles for WSS and turbulent kinetic energy (TKE) were derived from the blood flow computations. RESULTS The profile of the blood flow at the cannula outlets is displayed in Fig. 2 for all cannula tip settings, indi-
cating the dispersive properties of the meshlike tips. Table 1 shows that for all ECC settings, the distribution of the blood flow to the aortic branches was similar to physiological flow conditions. In order to comparatively examine the sandblasting effect of different cannula tip shapes, aortic WSS profiles were analyzed for each ECC setting. In general, the highest WSS values occurred in the area around the spot at which the cannula jet stream hit the aortic wall. In the case of straight cannulas, the primarily affected area was the posterior wall of the ascending aorta, while bent cannulas directed the outflow jet toward the orifice of the brachiocephalic
TABLE 1. Distribution of blood flow (%) among the aortic branches by ECC setting Aortic branch B C D E F G H I K
Straight dispersive
Straight end-hole
Bent dispersive
Bent end-hole
Physiological flow
15.70 7.85 7.85 16.02 10.67 10.68 10.68 10.27 10.27
15.64 7.83 7.81 16.00 10.66 10.66 10.66 10.36 10.36
15.81 7.90 7.87 16.11 10.74 10.39 10.39 10.39 10.39
16.12 7.91 7.86 15.59 10.39 10.77 10.78 10.29 10.29
15.80 7.90 7.90 15.80 10.53 10.53 10.53 10.53 10.53
B, brachiocephalic trunk; C, left common carotid artery; D, left subclavian artery; E, celiac trunk; F, superior mesenteric artery; G, left renal artery; H, right renal artery; I, left common iliac artery; K, right common iliac artery. Artif Organs, Vol. 39, No. 3, 2015
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FIG. 3. WSS profiles resulting from nonpulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C), and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. WSS given in pascals.
trunk. Dispersive cannula tips remarkably reduced the area of enhanced WSS as compared with controls, whereas bent tips further diminished the stressed region. These observations applied to simulations of nonpulsatile (Fig. 3) as well as pulsatile (Figs. 4 and 5) ECC. For bent and straight tip shapes, dispersive geometries reduced not only the spatial extent but also the absolute amount of WSS exerted on the aortic walls: The maximum values for nonpulsatile ECC as well as for the average and peak WSS during pulsatile ECC were diminished by approximately 50% (Table 2). Moreover, dispersive cannulas shortened the time period of enhanced WSS in each cardiac cycle of pulsatile simulations. Enhanced TKE was observed in the same areas as increased WSS. The spatial extent as well as the maximum values of increased TKE were reduced by dispersive cannulas under pulsatile and nonpulsatile conditions (Fig. 6; Table 3). DISCUSSION In order to examine the influence of dispersive arterial cannula tips on the local aortic WSS profiles, a recently validated numerical approach for simulating the effect of ECC on the human aortic blood flow was applied (4,5). For pulsatile and nonpulsatile ECC, straight as well as bent dispersive tips were Artif Organs, Vol. 39, No. 3, 2015
shown to reduce the spatial and temporal extent as well as the maximum values of local WSS in the cannulated aorta, as compared with control cannulas with end-hole tips. Endothelial and blood cell damage ECC is a mandatory tool for many operative techniques in cardiac surgery, including proximal aortic surgery, heart transplantation, heart valve repair, and conventional replacement. For patients with coronary artery disease, off-pump coronary artery bypass grafting (OPCAB) is an epidemiologically important approach to avoiding ECC during coronary surgery. Although recent clinical trials have suggested a benefit of OPCAB regarding intraoperative stroke, the long-term outcome including mortality and myocardial infarction was not improved as compared with bypass surgery under ECC (15–18). Therefore, ECC remains an indispensable standard technique in cardiac surgery, and intensified research on decreasing the risk of ECC-associated complications is warranted. Arterial embolization of atherosclerotic plaques is a common event during ECC and frequently results in severe complications, such as stroke or ischemia of other organs such as kidney, liver, or intestine. The sandblastlike effect of conventional arterial ECC cannulas is a major risk factor of endothelial damage
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FIG. 4. Average WSS profiles resulting from pulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C), and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. WSS given in pascals.
and plaque mobilization. Enhanced arterial WSS caused by the cannula jet stream is known to induce endothelial damage. After 120-min cardiopulmonary bypass in a porcine model, endothelial lesions in primarily healthy intima have been reported (1). While
chronic increase of WSS seems to prevent the development of atherosclerotic plaques, high values have been observed to be colocalized with unstable or ruptured plaques (2,3,19). Intraoperative stroke is one of the major adverse consequences of plaque
FIG. 5. Maximum WSS profiles resulting from pulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C), and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. WSS given in pascals.
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A. ASSMANN ET AL. TABLE 2. Maximum values of aortic WSS by shape of the aortic cannula tip WSS (Pa) Cannula tip shape
Nonpulsatile perfusion*
Pulsatile perfusion†
Straight dispersive Straight end-hole Bent dispersive Bent end-hole
22 37 16 34
20/110 40/250 23/132 43/227
* Mean values. † Mean values/peak values.
delamination. As up to 10% of all cardiosurgical patients, and up to 16% in high-risk groups, exhibit neurological complications after ECC, the prevention of plaque embolization is of major interest not only with regard to the individual patient but also due to economic aspects (20). With the aim of reducing the sandblasting effect of conventional end-hole-tip cannulas, different cannula geometries have been developed. Jet stream dispersion has been achieved by dispersive meshlike and funnel-shaped tips as well as by spininducing stators in the main bodies of arterial ECC cannulas. In mock circulation experiments, these cannulas have been shown to provide lower pressure gradients, back-pressure values, and strain-rate tensors than conventional end-hole-tip cannulas (8,9,21,22). Recently, a numerical study on cannulas with diffuser-cone tips resulted in improved WSS conditions in the aortic arch as compared to endhole tips (23). Numerical analysis of a similar dif-
fuser cannula geometry additionally pointed to reduced risk of hemolysis (24). Our present study shows the hemodynamic superiority of straight as well as bent cannulas with dispersive meshlike tips. A major advantage of this approach over recently published designs is that the tip of the cannula is pointed, while the recently reported diffuser cannulas exhibit divergent walls at the tip. Practical application, that is, insertion of such cannulas with divergent walls into arteries, has to be regarded as very critical, as at the end of the insertion process, the diameter of the hole that has to be created in the artery in order to introduce the broad tip will be larger than the diameter of the cannula at the level of the artery wall. This will subsequently result in arterial bleeding from the insertion site. In contrast, the pointed-tipped cannula used in the present study occludes the insertion hole in the arterial wall, thus preventing bleeding from the insertion site, as is known from clinical application of this cannula.
FIG. 6. Maximum TKE profiles resulting from pulsatile perfusion via straight dispersive (A), straight end-hole (B), bent dispersive (C). and bent end-hole (D) cannulas. View on the posterior aortic wall opposite to the cannulation site. TKE given in m2/s2.
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DISPERSIVE AORTIC CANNULAS REDUCE SHEAR TABLE 3. Maximum values of aortic TKE during pulsatile perfusion by shape of aortic cannula tip Cannula tip shape
TKE (m2/s2)
Straight dispersive Straight end-hole Bent dispersive Bent end-hole
0.408 0.992 0.362 0.780
The validity of the present computations was improved by applying a recently developed numerical model of ECC simulations based on loss coefficients as aortic boundary conditions (5). In a previous study, we had shown a remarkable decrease of WSS during nonpulsatile ECC as compared with pulsatile perfusion (4). The present data confirm this observation and reveal the independent WSS-lowering effect of dispersive cannulas under pulsatile as well as nonpulsatile ECC conditions. In both ECC scenarios, the maximum values of average WSS resulting from dispersive cannula perfusion were similar to the maximum values under physiological blood flow obtained in our previous study. The best hemodynamic performance regarding potential endothelial damage was observed when simulating bent dispersive tips, although, due to the geometry of the cannula with its flat body–tip angle, the resulting blood flow at the cannula outlet was not directed parallel to the aorta, and thus, it hit the aortic wall very close to the outlet, leaving room for further improvement of the cannula design. In contrast, the end-hole control cannula was placed in an ideal position in the center of the aortic lumen, generating a jet stream more parallel to the aortic walls. As a consequence, the distance between the cannula outlet and the site at which the jet stream hit the aortic wall was larger for the control cannula, which may have diminished the WSS exerted on the aorta as compared with the dispersive cannula, for which there was a very short distance between outlet and impact site on the aortic wall. That the dispersive cannula showed better performance in spite of the less beneficial outlet orientation and outlet–wall distance suggests that the level of WSS evoked by dispersive cannulas is not sensitive to displacement of the cannula. This aspect is of actual clinical relevance, as even in the case of thorough initial cannula positioning, at least slight displacement of the cannula frequently occurs during the operation. The reduction of WSS by dispersive cannulas is all the more noteworthy, as the primarily affected areas are the posterior wall of the ascending aorta (in the case of straight cannulas) and the orifice of the brachiocephalic trunk (in the case of bent cannulas). Both regions exhibit a high prevalence of plaque for-
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mation in atherosclerotic patients (25,26). Therefore, decreasing the local WSS during ECC might have high clinical impact. Besides WSS, the extent of TKE was also diminished by utilizing dispersive cannulas. As turbulent flow is known to increase blood cell damage (27), dispersive meshlike tips might be preferable not only to prevent endothelial damage and plaque embolization but also in terms of hemolysis during ECC. In addition, more uniform flow distribution originating from dispersive cannulas might beneficially affect organ perfusion. In a previous study, it was shown that owing to the Venturi effect, the jet stream of a regular end-hole cannula can severely impede the flow to the aortic branches (6). Dispersion of the cannula stream may reduce this effect, increase the pressure in the near field of the stream, and thus prevent malperfusion of branches that are located very close to the outlet of the cannula. Clinical data on the effect of aortic cannula design Despite the significance of reducing intraoperative plaque embolization during ECC, only a small number of clinical studies on the effect of aortic cannula design on ECC-associated complications exists so far. Weinstein et al. analyzed data from coronary artery bypass grafting (CABG) patients with intraoperative stroke and found predominantly lefthemispheric locations. As they could show that the utilized end-hole cannulas caused a high-velocity jet toward the orifice of the left common carotid artery, and aortic manipulation—for example by crossclamping, which is another possible risk factor of stroke—is believed to preferentially induce embolization into the contiguous brachiocephalic trunk, the investigators concluded that the cannula jet stream was a major reason for the occurrence of stroke (28). In 137 stroke patients after CABG, aortic cannulas with bent tips have been shown to significantly reduce the incidence as well as the severity of strokes as compared to straight cannulas (29). An echocardiographic study on the outlet flow profile of different aortic cannulas in humans revealed significantly reduced velocities for dispersive cannulas versus nondispersive models (30). A small case series evaluating diffuser-tip cannulas in CABG patients showed a diminished risk of cerebral gaseous and particle emboli when compared with previous data on standard end-hole cannulas (31). In summary, the existing literature suggests a beneficial effect of dispersive cannulas on the occurrence of intraoperative stroke during ECC. However, the clinical evidence is quite restricted, and randomized Artif Organs, Vol. 39, No. 3, 2015
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controlled trials examining the actual potential of dispersive aortic cannulas are warranted. Limitations of the study The distensibility of the physiological human aortic wall, which might influence blood flow profiles during pulsatile ECC, has not been considered in this study. However, the simulations are focused on patients with severe atherosclerosis, who account for the majority of cardiosurgical patients nowadays. Atherosclerotic and arteriosclerotic wall remodeling in the elderly leads to increased wall thickness and structural damage, both contributing to enhanced wall stiffness (32). In these patients, aortic wall distensibility is either lost or locally impaired in a heterogeneous pattern, which strongly impedes any attempt to simulate their individual profile of wall distensibility. As an idealized aortic geometry was utilized, the current approach allows for a general comparative examination of dispersive versus standard cannula tips. However, future MRI-supported animal ECC studies will have to reveal the effect of dispersive cannulas on the WSS profiles as well as on the resulting biological effect on the endothelium in individualized aortic geometries. CONCLUSIONS Based on our recently developed and validated numerical model for simulating the effect of extracorporeal circulation on human aortic blood flow, the present study shows that straight as well as bent arterial cannulas with meshlike dispersive tips improve aortic wall shear stress and turbulence profiles. Moreover, this effect was observed to be independent of whether pulsatile or nonpulsatile flow was applied. Thus, dispersive cannulas have the potential to reduce ECC-related complications such as stroke, endothelial damage, and hemolysis. Acknowledgments: The authors gratefully acknowledge Sorin Group (Milan, Italy) for financial support of this project. The study sponsor did not influence study design, collection, analysis or interpretation of data, writing of the manuscript, or the decision to submit the manuscript for publication. Conflict of Interest: None. REFERENCES 1. Schnürer C, Hager M, Györi G, et al. Evaluation of aortic cannula jet lesions in a porcine cardiopulmonary bypass (CPB) model. J Cardiovasc Surg 2011;52:105–9.
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