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Research Papers

Computational Study of Pulmonary Flow Patterns After Repair of Transposition of Great Arteries

[+] Author and Article Information
Francesco Capuano

Department of Industrial Engineering,
Università di Napoli Federico II,
Napoli 80125, Italy
e-mail: francesco.capuano@unina.it

Yue-Hin Loke

Division of Cardiology,
Children's National Health System,
Washington, DC 20010
e-mail: yloke@childrensnational.org

Ileen Cronin

Division of Cardiology,
Children's National Health System,
Washington, DC 20010
e-mail: icronin@childrensnational.org

Laura J. Olivieri

Division of Cardiology,
The Sheikh Zayed Institute for
Pediatric Surgical Innovation,
Children's National Health System,
Washington, DC 20010
e-mail: lolivieri@childrensnational.org

Elias Balaras

Department of Mechanical and
Aerospace Engineering,
George Washington University,
Washington, DC 20052
e-mail: balaras@gwu.edu

1Corresponding author.

Manuscript received September 18, 2018; final manuscript received February 19, 2019; published online March 25, 2019. Assoc. Editor: Ching-Long Lin.

J Biomech Eng 141(5), 051008 (Mar 25, 2019) (10 pages) Paper No: BIO-18-1414; doi: 10.1115/1.4043034 History: Received September 18, 2018; Revised February 19, 2019

Patients that undergo the arterial switch operation (ASO) to repair transposition of great arteries (TGA) can develop abnormal pulmonary trunk morphology with significant long-term complications. In this study, cardiovascular magnetic resonance was combined with computational fluid dynamics to investigate the impact of the postoperative layout on the pulmonary flow patterns. Three ASO patients were analyzed and compared to a volunteer control. Results showed the presence of anomalous shear layer instabilities, vortical and helical structures, and turbulent-like states in all patients, particularly as a consequence of the unnatural curvature of the pulmonary bifurcation. Streamlined, mostly laminar flow was instead found in the healthy subject. These findings shed light on the correlation between the post-ASO anatomy and the presence of altered flow features, and may be useful to improve surgical planning as well as the long-term care of TGA patients.

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References

Villafañe, J. , Lantin-Hermoso, M. R. , Bhatt, A. B. , Tweddell, J. S. , Geva, T. , Nathan, M. , Elliott, M. J. , Vetter, V. L. , Paridon, S. M. , Kochilas, L. , Jenkins, K. J. , Beekman, R. H. , Wernovsky, G. , and Towbin, J. A. , 2014, “ D-Transposition of the Great Arteries: The Current Era of the Arterial Switch Operation,” J. Am. Coll. Cardiol., 64(5), pp. 498–511. [CrossRef] [PubMed]
Shaher, R. M. , 1964, “ Complete and Inverted Transposition of the Great Vessels,” Br. Heart J., 26(1), p. 51. [CrossRef] [PubMed]
Jatene, A. , Fontes, V. , Paulista, P. , Souza, L. , Neger, F. , Galantier, M. , and Sousa, J. , 1976, “ Anatomic Correction of Transposition of the Great Vessels,” J. Thorac. Cardiovasc. Surg., 72(3), pp. 364–370. https://www.ncbi.nlm.nih.gov/pubmed/957754 [PubMed]
Senning, Å. , 1959, “ Surgical Correction of Transposition of the Great Vessels,” Surgery, 45(6), pp. 966–980. [PubMed]
Mustard, W. , 1964, “ Successful Two-Stage Correction of Transposition of the Great Vessels,” Surgery, 55(3), pp. 469–472. [PubMed]
Fraser, C. D. , 2017, “ The Neonatal Arterial Switch Operation: Technical Pearls,” Semin. Thorac. Cardiovasc. Surg.:Pediatr. Card. Surg. Annu., 20, pp. 38–42. https://www.sciencedirect.com/science/article/pii/S1092912616300278?via%3Dihub
Lecompte, Y. , Zannini, L. , Hazan, E. , Jarreau, M. , Bex, J. , Tu, T. V. , and Neveux, J. , 1981, “ Anatomic Correction of Transposition of the Great Arteries,” J. Thorac. Cardiovasc. Surg., 82(4), pp. 629–631. https://www.ncbi.nlm.nih.gov/pubmed/7278356 [PubMed]
Khairy, P. , Clair, M. , Fernandes, S. M. , Blume, E. D. , Powell, A. J. , Newburger, J. W. , Landzberg, M. J. , and Mayer, J. E. , 2013, “ Cardiovascular Outcomes After the Arterial Switch Operation for D-Transposition of the Great Arteries,” Circulation, 127(3), pp. 331–339. [CrossRef] [PubMed]
Raju, V. , Burkhart, H. M. , Durham , L. A., III , Eidem, B. W. , Phillips, S. D. , Li, Z. , Schaff, H. V. , and Dearani, J. A. , 2013, “ Reoperation After Arterial Switch: A 27-Year Experience,” Ann. Thorac. Surg., 95(6), pp. 2105–2113. [CrossRef] [PubMed]
Gutberlet, M. , Boeckel, T. , Hosten, N. , Vogel, M. , Kühne, T. , Oellinger, H. , Ehrenstein, T. , Venz, S. , Hetzer, R. , Bein, G. , and Felix, R. , 2000, “ Arterial Switch Procedure for D-Transposition of the Great Arteries: Quantitative Midterm Evaluation of Hemodynamic Changes With Cine MR Imaging and Phase-Shift Velocity Mapping-Initial Experience,” Radiology, 214(2), pp. 467–475. [CrossRef] [PubMed]
Morgan, C. T. , Mertens, L. , Grotenhuis, H. , Yoo, S.-J. , Seed, M. , and Grosse-Wortmann, L. , 2017, “ Understanding the Mechanism for Branch Pulmonary Artery Stenosis After the Arterial Switch Operation for Transposition of the Great Arteries,” Eur. Heart J. Cardiovasc. Imaging, 18(2), pp. 180–185. [CrossRef] [PubMed]
Ntsinjana, H. N. , Capelli, C. , Biglino, G. , Cook, A. C. , Tann, O. , Derrick, G. , Taylor, A. M. , and Schievano, S. , 2014, “ 3D Morphometric Analysis of the Arterial Switch Operation Using In Vivo MRI Data,” Clin. Anat., 27(8), pp. 1212–1222. [CrossRef] [PubMed]
Geiger, J. , Hirtler, D. , Bürk, J. , Stiller, B. , Arnold, R. , Jung, B. , Langer, M. , and Markl, M. , 2014, “ Postoperative Pulmonary and Aortic 3D Haemodynamics in Patients After Repair of Transposition of the Great Arteries,” Eur. Radiol., 24(1), pp. 200–208. [CrossRef] [PubMed]
Massin, M. , Nitsch, G. , Däbritz, S. , Seghaye, M.-C. , Messmer, B. , and Von Bernuth, G. , 1998, “ Growth of Pulmonary Artery After Arterial Switch Operation for Simple Transposition of the Great Arteries,” Eur. J. Pediatr., 157(2), pp. 95–100. [CrossRef] [PubMed]
Chiu, S. , Lee, M.-L. , Huang, S.-C. , Chang, C.-I. , Chen, Y.-S. , Wu, M.-H. , and Anderson, R. H. , 2016, “ The Concept of the Arch Window in the Spiral Switch of the Great Arteries,” Pediatr. Cardiol., 37(6), pp. 1153–1161. [CrossRef] [PubMed]
Riesenkampff, E. , Nordmeyer, S. , Al-Wakeel, N. , Kropf, S. , Kutty, S. , Berger, F. , and Kuehne, T. , 2014, “ Flow-Sensitive Four-Dimensional Velocity-Encoded Magnetic Resonance Imaging Reveals Abnormal Blood Flow Patterns in the Aorta and Pulmonary Trunk of Patients With Transposition,” Cardiol. Young, 24(1), pp. 47–53. [CrossRef] [PubMed]
Markl, M. , Kilner, P. J. , and Ebbers, T. , 2011, “ Comprehensive 4D Velocity Mapping of the Heart and Great Vessels by Cardiovascular Magnetic Resonance,” J. Cardiovasc. Magn. Reson., 13(1), p. 7. [CrossRef] [PubMed]
Sievers, H.-H. , Putman, L. M. , Kheradvar, A. , Gabbert, D. , Wegner, P. , Scheewe, J. , Salehi-Ravesh, M. , Kramer, H.-H. , and Rickers, C. , 2016, “ 4D Flow Streamline Characteristics of the Great Arteries Twenty Years After Lecompte and Direct Spiral Arterial Switch Operation (DSASO) in Simple TGA,” Global Cardiol. Sci. Pract., 2016(3), p. e201629.
Tang, T. , Chiu, S. , Chen, H.-C. , Cheng, K.-Y. , and Chen, S.-J. , 2001, “ Comparison of Pulmonary Arterial Flow Phenomena in Spiral and Lecompte Models by Computational Fluid Dynamics,” J. Thorac. Cardiovasc. Surg., 122(3), pp. 529–534. [CrossRef] [PubMed]
Rickers, C. , Kheradvar, A. , Sievers, H.-H. , Falahatpisheh, A. , Wegner, P. , Gabbert, D. , Jerosch-Herold, M. , Hart, C. , Voges, I. , Putman, L. M. , Kristo, I. , Fischer, G. , Scheewe, J. , and Kramer, H.-H. , 2016, “ Is the Lecompte Technique the Last Word on Transposition of the Great Arteries Repair for All Patients? A Magnetic Resonance Imaging Study Including a Spiral Technique Two Decades Postoperatively,” Interact. Cardiovasc. Thorac. Surg., 22(6), pp. 817–825. [CrossRef] [PubMed]
Morris, P. D. , Narracott, A. , von Tengg-Kobligk, H. , Silva Soto, D. A. , Hsiao, S. , Lungu, A. , Evans, P. , Bressloff, N. W. , Lawford, P. V. , Hose, D. R. , and Gunn, J. P. , 2016, “ Computational Fluid Dynamics Modelling in Cardiovascular Medicine,” Heart, 102(1), pp. 18–28. [CrossRef] [PubMed]
Zhong, L. , Zhang, J.-M. , Su, B. , San Tan, R. , Allen, J. C. , and Kassab, G. S. , 2018, “ Application of Patient-Specific Computational Fluid Dynamics in Coronary and Intra-Cardiac Flow Simulations: Challenges and Opportunities,” Front. Physiol., 9, p. 742. [CrossRef] [PubMed]
Henk, C. B. , Schlechta, B. , Grampp, S. , Gomischek, G. , Klepetko, W. , and Mostbeck, G. H. , 1998, “ Pulmonary and Aortic Blood Flow Measurements in Normal Subjects and Patients After Single Lung Transplantation at 0.5 T Using Velocity Encoded Cine MRI,” Chest, 114(3), pp. 771–779. [CrossRef] [PubMed]
Updegrove, A. , Wilson, N. M. , Merkow, J. , Lan, H. , Marsden, A. L. , and Shadden, S. C. , 2017, “ Simvascular: An Open Source Pipeline for Cardiovascular Simulation,” Ann. Biomed. Eng., 45(3), pp. 525–541. [CrossRef] [PubMed]
Kung, E. O. , Les, A. S. , Figueroa, C. A. , Medina, F. , Arcaute, K. , Wicker, R. B. , McConnell, M. V. , and Taylor, C. A. , 2011, “ In Vitro Validation of Finite Element Analysis of Blood Flow in Deformable Models,” Ann. Biomed. Eng., 39(7), pp. 1947–1960. [CrossRef] [PubMed]
Kung, E. , Kahn, A. M. , Burns, J. C. , and Marsden, A. , 2014, “ In Vitro Validation of Patient-Specific Hemodynamic Simulations in Coronary Aneurysms Caused by Kawasaki Disease,” Cardiovasc. Eng. Technol., 5(2), pp. 189–201. [CrossRef] [PubMed]
Whiting, C. H. , and Jansen, K. E. , 2001, “ A Stabilized Finite Element Method for the Incompressible Navier-Stokes Equations Using a Hierarchical Basis,” Int. J. Numer. Methods Fluids, 35(1), pp. 93–116. [CrossRef]
Moghadam, M. E. , Bazilevs, Y. , Hsia, T.-Y. , Vignon-Clementel, I. E. , and Marsden, A. L. , 2011, “ A Comparison of Outlet Boundary Treatments for Prevention of Backflow Divergence With Relevance to Blood Flow Simulations,” Comput. Mech., 48(3), pp. 277–291. [CrossRef]
Schiavazzi, D. E. , Kung, E. O. , Marsden, A. L. , Baker, C. , Pennati, G. , Hsia, T.-Y. , Hlavacek, A. , and Dorfman, A. L. , Modeling of Congenital Hearts Alliance (MOCHA) Investigators, 2015, “ Hemodynamic Effects of Left Pulmonary Artery Stenosis After Superior Cavopulmonary Connection: A Patient-Specific Multiscale Modeling Study,” J. Thorac. Cardiovasc. Surg., 149(3), pp. 689–696. [CrossRef] [PubMed]
Tang, B. T. , Fonte, T. A. , Chan, F. P. , Tsao, P. S. , Feinstein, J. A. , and Taylor, C. A. , 2011, “ Three-Dimensional Hemodynamics in the Human Pulmonary Arteries Under Resting and Exercise Conditions,” Ann. Biomed. Eng., 39(1), pp. 347–358. [CrossRef] [PubMed]
Morgan, V. L. , Roselli, R. J. , and Lorenz, C. H. , 1998, “ Normal Three-Dimensional Pulmonary Artery Flow Determined by Phase Contrast Magnetic Resonance Imaging,” Ann. Biomed. Eng., 26(4), pp. 557–566. [CrossRef] [PubMed]
Vignon-Clementel, I. E. , Figueroa, C. A. , Jansen, K. E. , and Taylor, C. A. , 2006, “ Outflow Boundary Conditions for Three-Dimensional Finite Element Modeling of Blood Flow and Pressure in Arteries,” Comput. Methods Appl. Mech. Eng., 195(29–32), pp. 3776–3796. [CrossRef]
Yang, W. , Feinstein, J. A. , and Vignon-Clementel, I. E. , 2016, “ Adaptive Outflow Boundary Conditions Improve Post-Operative Predictions After Repair of Peripheral Pulmonary Artery Stenosis,” Biomech. Model. Mechanobiol., 15(5), pp. 1345–1353. [CrossRef] [PubMed]
Hunt, J. , Wray, A. , and Moin, P. , 1988, “ Eddies, Streams, and Convergence Zones in Turbulent Flows,” Technical Report, Center for Turbulence Research, Stanford, CA, Report No. CTR-S88.
Dean, W. , 1928, “ The Stream-Line Motion of Fluid in a Curved Pipe,” London, Edinburgh Dublin Philos. Mag. J. Sci., 5(30), pp. 673–695. [CrossRef]
Berger, S. , Talbot, L. , and Yao, L. , 1983, “ Flow in Curved Pipes,” Annu. Rev. Fluid Mech., 15(1), pp. 461–512. [CrossRef]
Kühnen, J. , Braunshier, P. , Schwegel, M. , Kuhlmann, H. , and Hof, B. , 2015, “ Subcritical Versus Supercritical Transition to Turbulence in Curved Pipes,” J. Fluid Mech., 770, p. R3. https://doi.org/10.1017/jfm.2015.184
Vester, A. K. , Örlü, R. , and Alfredsson, P. H. , 2016, “ Turbulent Flows in Curved Pipes: Recent Advances in Experiments and Simulations,” ASME Appl. Mech. Rev., 68(5), p. 050802. [CrossRef]
Ku, D. N. , 1997, “ Blood Flow in Arteries,” Annu. Rev. Fluid Mech., 29(1), pp. 399–434. [CrossRef]
Chern, M.-J. , Wu, M.-T. , and Her, S.-W. , 2012, “ Numerical Study for Blood Flow in Pulmonary Arteries After Repair of Tetralogy of Fallot,” Comput. Math. Methods Med., 2012, p. 198108. [CrossRef]
Chern, M.-J. , Wu, M.-T. , and Wang, H.-L. , 2008, “ Numerical Investigation of Regurgitation Phenomena in Pulmonary Arteries of Tetralogy of Fallot Patients After Repair,” J. Biomech., 41(14), pp. 3002–3009. [CrossRef] [PubMed]
Zhang, W. , Liu, J. , Yan, Q. , Liu, J. , Hong, H. , and Mao, L. , 2016, “ Computational Haemodynamic Analysis of Left Pulmonary Artery Angulation Effects on Pulmonary Blood Flow,” Interact. Cardiovasc. Thorac. Surg., 23(4), pp. 519–525. [CrossRef] [PubMed]
Hanna, B. D. , 2005, “ Blood Flow in Normal and Diseased Pulmonary Arteries,” Ventricular Function and Blood Flow in Congenital Heart Disease, M. A. Fogel, ed., Wiley-Blackwell, Hoboken, NJ, pp. 275–285.
Zhong, L. , Su, Y. , Yeo, S.-Y. , Tan, R.-S. , Ghista, D. N. , and Kassab, G. , 2009, “ Left Ventricular Regional Wall Curvedness and Wall Stress in Patients With Ischemic Dilated Cardiomyopathy,” Am. J. Physiol. Heart Circ. Physiol., 296(3), pp. H573–H584. [CrossRef] [PubMed]
Bruse, J. L. , Khushnood, A. , McLeod, K. , Biglino, G. , Sermesant, M. , Pennec, X. , Taylor, A. M. , Hsia, T.-Y. , Schievano, S. , Taylor, A. M. , Khambadkone, S. , Schievano, S. , de Leval, M. , Hsia, T.-Y. , Bove, E. , Dorfman, A. , Baker, G. H. , Hlavacek, A. , Migliavacca, F. , Pennati, G. , Dubini, G. , Marsden, A. , Vignon-Clementel, I. , and Figliola, R. , 2017, “ How Successful Is Successful? Aortic Arch Shape After Successful Aortic Coarctation Repair Correlates With Left Ventricular Function,” J. Thorac. Cardiovasc. Surg., 153(2), pp. 418–427. [CrossRef] [PubMed]
Lee, S. E. , Lee, S.-W. , Fischer, P. F. , Bassiouny, H. S. , and Loth, F. , 2008, “ Direct Numerical Simulation of Transitional Flow in a Stenosed Carotid Bifurcation,” J. Biomech., 41(11), pp. 2551–2561. [CrossRef] [PubMed]
Varghese, S. S. , Frankel, S. H. , and Fischer, P. F. , 2007, “ Direct Numerical Simulation of Stenotic Flows—Part 2: Pulsatile Flow,” J. Fluid Mech., 582, pp. 281–318. [CrossRef]
Liu, X. , Sun, A. , Fan, Y. , and Deng, X. , 2015, “ Physiological Significance of Helical Flow in the Arterial System and Its Potential Clinical Applications,” Ann. Biomed. Eng., 43(1), pp. 3–15. [CrossRef] [PubMed]
Ku, J. P. , Draney, M. T. , Arko, F. R. , Lee, W. A. , Chan, F. P. , Pelc, N. J. , Zarins, C. K. , and Taylor, C. A. , 2002, “ In Vivo Validation of Numerical Prediction of Blood Flow in Arterial Bypass Grafts,” Ann. Biomed. Eng., 30(6), pp. 743–752. [CrossRef] [PubMed]
Bächler, P. , Pinochet, N. , Sotelo, J. , Crelier, G. , Irarrazaval, P. , Tejos, C. , and Uribe, S. , 2013, “ Assessment of Normal Flow Patterns in the Pulmonary Circulation by Using 4D Magnetic Resonance Velocity Mapping,” Magn. Resonance Imaging, 31(2), pp. 178–188. [CrossRef]
Chiu, I.-S. , Huang, S.-C. , Chen, Y.-S. , Chang, C.-I. , Lee, M.-L. , Chen, S.-J. , Chen, M.-R. , and Wu, M.-H. , 2010, “ Restoring the Spiral Flow of Nature in Transposed Great Arteries,” Eur. J. Cardio-Thorac. Surg., 37(6), pp. 1239–1245. [CrossRef]
Kheyfets, V. O. , O'Dell, W. , Smith, T. , Reilly, J. J. , and Finol, E. A. , 2013, “ Considerations for Numerical Modeling of the Pulmonary Circulation—A Review With a Focus on Pulmonary Hypertension,” ASME J. Biomech. Eng., 135(6), p. 061011. [CrossRef]
Zambrano, B. A. , McLean, N. A. , Zhao, X. , Tan, J.-L. , Zhong, L. , Figueroa, C. A. , Lee, L. C. , and Baek, S. , 2018, “ Image-Based Computational Assessment of Vascular Wall Mechanics and Hemodynamics in Pulmonary Arterial Hypertension Patients,” J. Biomech., 68, pp. 84–92. [CrossRef] [PubMed]
Perktold, K. , and Rappitsch, G. , 1995, “ Computer Simulation of Local Blood Flow and Vessel Mechanics in a Compliant Carotid Artery Bifurcation Model,” J. Biomech., 28(7), pp. 845–856. [CrossRef] [PubMed]

Figures

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Fig. 1

Comparison of healthy (a), pre-ASO (b), and post-ASO (c) arrangement of the great arteries shown by reconstructed patient-specific models. In the pre-ASO case (b), two separate circulatory systems are created: the right ventricle (RV) receives deoxygenated blood and pumps it back to the body via the ascending aorta (AAo), while the LV continuously exchanges oxygen-rich blood with the pulmonary circulation. After ASO (c), the coupling is restored although the PT wraps around the ascending aorta, leading to significant changes in morphology as compared to the physiological spiral anatomy (a).

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Fig. 2

Main geometric differences between healthy and post-ASO pulmonary arteries. Alterations are highlighted for the post-ASO geometry.

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Fig. 3

Segmentation, 3D modeling, meshing process, and boundary conditions. (a) The blood pool representing the pulmonary arteries is identified and segmented by drawing a contour to create an overlying mask. (b) The segmented mask is then converted over to a 3D digital model in STL format. In this example, the right ventricle is also included as part of the initial model created. (c) 3D editing is performed to fine anatomic inlets and anatomic outlets. The outlets are cut as distally as allowed to create second-order branching. (d) From left to right: frontal, lateral, and top view of the four models obtained via segmentation process. In the top view, the locations of the cut planes considered in the Results section are reported. (e) Exemplary mesh (patient 1); the inset illustrates a detailed view of the surface mesh. (f) Inlet flow rates for the four models; shown are also characteristic points of the cardiac cycle considered in the results section.

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Fig. 4

Comparison of CFD results to clinical data. (Left) Phase-averaged time signal of pressure in MPA, RPA and LPA; T is the cardiac cycle period. (Right) Phase-averaged streamwise velocity along a line moving from the inner wall to the outer wall of the RPA within the phase-contrast cut plane.

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Fig. 5

Snapshot of the flow structure for the four subjects at peak systole. (top row) Vortical structures identified by isosurfaces of Q =0.05Qmax colored by normalized helicity; (middle row) streamlines colored by velocity magnitude; (bottom row) wall shear stress.

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Fig. 6

Normal-to-plane vorticity contours in the planes identified in the top row picture (patient 1). From top to bottom: mid-acceleration, peak systole, and mid-deceleration. Contour lines are plotted for ω∈ [±250, ±500, ±1000, ±1500, ±2000].

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Fig. 7

Phase-averaged velocity fields at peak systole (top row) and mid deceleration (bottom row) for patient 1. Superimposed are in-plane phase-averaged velocity vectors. Cross sections are not to scale.

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Fig. 8

Phase-averaged square-root of turbulent kinetic energy at peak systole (top row) and mid-deceleration (bottom row) for patient 1. Cross sections are not to scale.

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Fig. 9

Phase-averaged square-root of turbulent kinetic energy at peak systole for all subjects

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Fig. 10

Illustrative definition of the radius of curvature of the bend between MPA and RPA. The radius is constructed on the post-ASO geometry; the healthy model is also shown for comparison.

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