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Published in: Pediatric Cardiology 3/2015

01-03-2015 | Original Article

Computational Fluid Dynamics Characterization of Blood Flow in Central Aorta to Pulmonary Artery Connections: Importance of Shunt Angulation as a Determinant of Shear Stress-Induced Thrombosis

Authors: Carey Celestin, Martin Guillot, Nancy Ross-Ascuitto, Robert Ascuitto

Published in: Pediatric Cardiology | Issue 3/2015

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Abstract

The central aortic shunt, consisting of a Gore-Tex (polytetrafluoroethylene) tube (graft) connecting the ascending aorta to the pulmonary artery, is a palliative operation for neonates with cyanotic congenital heart disease. These tubes often have an extended length, and therefore must be angulated to complete the connection to the posterior pulmonary arteries. Thrombosis of the graft is not uncommon and can be life-threatening. We have shown that a viscous fluid (such as blood) traversing a curve or bend in a small-caliber vessel or conduit can give rise to marked increases in wall shear stress, which is the major mechanical factor responsible for vascular thrombosis. Thus, the objective of this study was to use computational fluid dynamics to investigate whether wall shear stress (and shear rate) generated in angulated central aorta-to-pulmonary artery connections, in vivo, can be of magnitude and distribution to initiate platelet activation/aggregation, ultimately leading to thrombus formation. Anatomical features required to construct the computer-simulated blood flow pathways were verified from angiograms of central aortic shunts in patients. For the modeled central aortic shunts, we found wall shear stresses of (80–200 N/m2), with shear rates of (16,000–40,000/s), at sites of even modest curvature, to be high enough to cause platelet-mediated shunt thrombosis. The corresponding energy losses for the fluid transitions through the aorta-to-pulmonary connections constituted (70 %) of the incoming flow’s mechanical energy. The associated velocity fields within these shunts exhibited vortices, eddies, and flow stagnation/recirculation, which are thrombogenic in nature and conducive to energy dissipation. Angulation-induced, shear stress-mediated shunt thrombosis is insensitive to aspirin therapy alone. Thus, for patients with central aortic shunts of longer length and with angulation, aspirin alone will provide insufficient protection against clotting. These patients are at risk for shunt thrombosis and significant morbidity and mortality, unless their anticoagulation regimen includes additional antiplatelet medications.
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Literature
1.
go back to reference Al Jubair KA, Al Fagih MR, Al Jarallah AS, Al Yousef S, All Khan MA, Ashmeg A, Al Faraldi Y, Sawyer W (1998) Results of 546 Blalock-Taussig shunts performed in 478 patients. Cardiol Young. 8(4):486–490CrossRefPubMed Al Jubair KA, Al Fagih MR, Al Jarallah AS, Al Yousef S, All Khan MA, Ashmeg A, Al Faraldi Y, Sawyer W (1998) Results of 546 Blalock-Taussig shunts performed in 478 patients. Cardiol Young. 8(4):486–490CrossRefPubMed
2.
go back to reference Amato JJ, Marbey ML, Bush C, Galdieri RJ, Cotroneo JV, Bushong J (1988) Systemic-pulmonary polytetrafluoroethylene shunts in palliative operations for congenital heart surgery. Revival of the central shunt. J Thorac Cardiovasc Surg. 95:62–69PubMed Amato JJ, Marbey ML, Bush C, Galdieri RJ, Cotroneo JV, Bushong J (1988) Systemic-pulmonary polytetrafluoroethylene shunts in palliative operations for congenital heart surgery. Revival of the central shunt. J Thorac Cardiovasc Surg. 95:62–69PubMed
3.
go back to reference Ascuitto RJ, Kydon DW, Ross-Ascuitto NT (2001) Pressure loss from flow energy dissipation: relevance to Fontan-type modifications. Pediatr Cardiol 22:110–115CrossRefPubMed Ascuitto RJ, Kydon DW, Ross-Ascuitto NT (2001) Pressure loss from flow energy dissipation: relevance to Fontan-type modifications. Pediatr Cardiol 22:110–115CrossRefPubMed
4.
go back to reference Ascuitto R, Ross-Ascuitto N, Guillot M (2010) Fluid Viscosity increases pressure drop and exacerbates flow-energy loss (Relevance to Modified-Fontan patients with elevated hematocrit). Congenit Cardiol Today 8(12):3–12 Ascuitto R, Ross-Ascuitto N, Guillot M (2010) Fluid Viscosity increases pressure drop and exacerbates flow-energy loss (Relevance to Modified-Fontan patients with elevated hematocrit). Congenit Cardiol Today 8(12):3–12
5.
go back to reference Barragry TP, Ring WS, Blatchford JW, Foker JE (1987) Central aorta-pulmonary artery shunts in neonates with complex cyanotic congenital heart disease. J Thorac Cardiovasc Surg. 93:767–774PubMed Barragry TP, Ring WS, Blatchford JW, Foker JE (1987) Central aorta-pulmonary artery shunts in neonates with complex cyanotic congenital heart disease. J Thorac Cardiovasc Surg. 93:767–774PubMed
6.
go back to reference Berger SA, Talbot L, Yao LS (1983) Flow in curved pipes. Ann Rev Fluid Mech 15:461–512CrossRef Berger SA, Talbot L, Yao LS (1983) Flow in curved pipes. Ann Rev Fluid Mech 15:461–512CrossRef
7.
go back to reference Bove EL, Sondheimer HM, Kavey REW, Byram CJ, Blackman MS, Parker FB Jr (1984) Subclavian-pulmonary artery shunts with polytetrafluoroethylene interposition grafts. Ann Thorac Surg 37:88–91CrossRefPubMed Bove EL, Sondheimer HM, Kavey REW, Byram CJ, Blackman MS, Parker FB Jr (1984) Subclavian-pulmonary artery shunts with polytetrafluoroethylene interposition grafts. Ann Thorac Surg 37:88–91CrossRefPubMed
8.
go back to reference Ciaravella JM, Midgley FM (1980) Construction of interposition polytetrafluoroethylene ascending aorta-pulmonary artery shunt. Ann Thorac Surg 29:570–572CrossRefPubMed Ciaravella JM, Midgley FM (1980) Construction of interposition polytetrafluoroethylene ascending aorta-pulmonary artery shunt. Ann Thorac Surg 29:570–572CrossRefPubMed
9.
go back to reference Cook NS, Kottirsch G, Zerwes H-G (1994) Platelet glycoprotein IIb/IIIa antagonists. Drugs Future. 19:135–159 Cook NS, Kottirsch G, Zerwes H-G (1994) Platelet glycoprotein IIb/IIIa antagonists. Drugs Future. 19:135–159
11.
go back to reference Dean WR (1927) Note on the motion of fluid in a curved pipe. Phil Mag J 20:208–223CrossRef Dean WR (1927) Note on the motion of fluid in a curved pipe. Phil Mag J 20:208–223CrossRef
12.
go back to reference Dean WR (1928) LXXII. The stream-line motion of fluid in a curved pipe (Second Paper). Phil Mag S 7 Ser 5(30):673–695CrossRef Dean WR (1928) LXXII. The stream-line motion of fluid in a curved pipe (Second Paper). Phil Mag S 7 Ser 5(30):673–695CrossRef
13.
go back to reference Donahoo JS, Gardner TJ, Zahka K, Kidd L (1980) Systemic-pulmonary shunts in neonates and infants using microporous expanded polytetrafluoroethylene: Immediate and late results. Ann Thorac Surg 30:146–150CrossRefPubMed Donahoo JS, Gardner TJ, Zahka K, Kidd L (1980) Systemic-pulmonary shunts in neonates and infants using microporous expanded polytetrafluoroethylene: Immediate and late results. Ann Thorac Surg 30:146–150CrossRefPubMed
14.
go back to reference Fruccone NJ, Bowman FO, Malm JR, Gersony WM (1974) Systemic-pulmonary arterial shunts in the first year of life. Circulation 49:508–511CrossRef Fruccone NJ, Bowman FO, Malm JR, Gersony WM (1974) Systemic-pulmonary arterial shunts in the first year of life. Circulation 49:508–511CrossRef
15.
go back to reference Gazzaniga AB, Elliott MP, Sperling DR et al (1976) Microporous expanded polytetrafluoroethylene arterial prosthesis for construction of aortopulmonary shunts; experimental and clinical results. Ann Thorac Surg 21:322–327CrossRefPubMed Gazzaniga AB, Elliott MP, Sperling DR et al (1976) Microporous expanded polytetrafluoroethylene arterial prosthesis for construction of aortopulmonary shunts; experimental and clinical results. Ann Thorac Surg 21:322–327CrossRefPubMed
16.
go back to reference Goto S, Salomon DR, Ikeda Y, Ruggeri ZM (1995) Characterization of the unique mechanisms mediating the shear-dependent binding of soluble von Willebrand factor to platelets. J Biol Chem 270:23353CrossRef Goto S, Salomon DR, Ikeda Y, Ruggeri ZM (1995) Characterization of the unique mechanisms mediating the shear-dependent binding of soluble von Willebrand factor to platelets. J Biol Chem 270:23353CrossRef
17.
go back to reference Guan X, Martonen TB (1997) Simulations of flow in curved tubes. Aerosol Sci Technol 26:485–504CrossRef Guan X, Martonen TB (1997) Simulations of flow in curved tubes. Aerosol Sci Technol 26:485–504CrossRef
18.
go back to reference Guillot M, Ross-Ascuitto N, Ascuitto R (2012) Fluid-flow energetics for curved or angulated pathways associated with staged operations for the modified Fontan procedure. Congenit Cardiol Today 10(1):2–14 Guillot M, Ross-Ascuitto N, Ascuitto R (2012) Fluid-flow energetics for curved or angulated pathways associated with staged operations for the modified Fontan procedure. Congenit Cardiol Today 10(1):2–14
19.
go back to reference Guyton RA, Owens JE, Waumett JD, Dooley KJ, Hatcher CR, Williams WH (1983) The Blalock-Taussig shunt. J Thorac Cardiovasc Surg 85:917–922PubMed Guyton RA, Owens JE, Waumett JD, Dooley KJ, Hatcher CR, Williams WH (1983) The Blalock-Taussig shunt. J Thorac Cardiovasc Surg 85:917–922PubMed
20.
go back to reference Hathcock JJ (2006) Flow effects on coagulation and thrombosis. Arterioscler Thromb Vasc Biol 26:1729–1737CrossRefPubMed Hathcock JJ (2006) Flow effects on coagulation and thrombosis. Arterioscler Thromb Vasc Biol 26:1729–1737CrossRefPubMed
21.
go back to reference Heyligers JMM, Verhagen HJM, Rotmans JI, Weeterings C, deGroot PG, Moll FL, Lisman T (2006) Heparin immobilization reduces thrombogenicity of small-caliber expanded polytetrafluoroethylene grafts. J Vasc Surg 43(3):587–591CrossRefPubMed Heyligers JMM, Verhagen HJM, Rotmans JI, Weeterings C, deGroot PG, Moll FL, Lisman T (2006) Heparin immobilization reduces thrombogenicity of small-caliber expanded polytetrafluoroethylene grafts. J Vasc Surg 43(3):587–591CrossRefPubMed
22.
go back to reference Holme PA, Orvim LL, Hamers MJAG, Solum NO, Brosstad FR, Barstad RM, Sakariassen KS (1997) Shear-induced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with severe stenosis. Arterioscler Thromb Vasc Biol 17:646–653CrossRefPubMed Holme PA, Orvim LL, Hamers MJAG, Solum NO, Brosstad FR, Barstad RM, Sakariassen KS (1997) Shear-induced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with severe stenosis. Arterioscler Thromb Vasc Biol 17:646–653CrossRefPubMed
23.
go back to reference Jennings RB, Innes BJ, Brickman RD (1978) Use of microporous expanded polytetrafluoroethylene grafts for aorta-pulmonary shunts in infants and complex cyanotic heart disease. J Thorac Cardiovasc Surg 76:489–494PubMed Jennings RB, Innes BJ, Brickman RD (1978) Use of microporous expanded polytetrafluoroethylene grafts for aorta-pulmonary shunts in infants and complex cyanotic heart disease. J Thorac Cardiovasc Surg 76:489–494PubMed
24.
go back to reference Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL (1996) Platelets and shear stress. Blood. 88:1525–1541PubMed Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL (1996) Platelets and shear stress. Blood. 88:1525–1541PubMed
25.
go back to reference Kulik TJ, Foker JE, Lucas RV, et al (1981) Post-operative hemodynamics in children with polytetrafluoroethylene shunts. Circulation 64(Pt 2):II123-130 Kulik TJ, Foker JE, Lucas RV, et al (1981) Post-operative hemodynamics in children with polytetrafluoroethylene shunts. Circulation 64(Pt 2):II123-130
26.
go back to reference Laks H, Fagan L, Barner HB, Willman VL (1978) The Blalock–Taussig shunt in the neonate. Ann Thorac Surg 25:220–224CrossRefPubMed Laks H, Fagan L, Barner HB, Willman VL (1978) The Blalock–Taussig shunt in the neonate. Ann Thorac Surg 25:220–224CrossRefPubMed
27.
go back to reference Lamberti JJ, Carlisle J, Waldman JD et al (1984) Systemic-pulmonary shunts in infants and children. J Thorac Cardiovasc Surg 88:76–81PubMed Lamberti JJ, Carlisle J, Waldman JD et al (1984) Systemic-pulmonary shunts in infants and children. J Thorac Cardiovasc Surg 88:76–81PubMed
28.
go back to reference Li JS, Yow E, Berezny KY, Rhodes JF, Bokesch PM, Charpie JR et al (2007) Clinical outcomes of palliative surgery including a systemic-to-pulmonary artery shunt in infants with cyanotic congenital heart disease. Does aspirin make a difference? Circulation. 116:293–297CrossRefPubMed Li JS, Yow E, Berezny KY, Rhodes JF, Bokesch PM, Charpie JR et al (2007) Clinical outcomes of palliative surgery including a systemic-to-pulmonary artery shunt in infants with cyanotic congenital heart disease. Does aspirin make a difference? Circulation. 116:293–297CrossRefPubMed
29.
go back to reference Maalej N, Folts JD (1996) Increased shear stress overcomes the antithrombotic platelet inhibitory effect of aspirin in stenosed dog coronary arteries. Circulation 93:1201–1205CrossRefPubMed Maalej N, Folts JD (1996) Increased shear stress overcomes the antithrombotic platelet inhibitory effect of aspirin in stenosed dog coronary arteries. Circulation 93:1201–1205CrossRefPubMed
30.
go back to reference Martin D, Zaman A, Hacker J, Mendelow D, Birchall D (2009) Analysis of haemodynamic factors involved in carotid atherosclerosis using computational fluid dynamics. Br J Radiol 82:S33–S38CrossRefPubMed Martin D, Zaman A, Hacker J, Mendelow D, Birchall D (2009) Analysis of haemodynamic factors involved in carotid atherosclerosis using computational fluid dynamics. Br J Radiol 82:S33–S38CrossRefPubMed
31.
go back to reference McCrary JK, Nolasco LH, Hellums JD, Kroll MH, Turner NA, Moake JL (1995) Direct demonstration of radiolabeled von Willebrand factor binding to platelet glycoprotein Ib and IIb–IIIa in the presence of shear stress. Ann Biomed Eng 23:787CrossRefPubMed McCrary JK, Nolasco LH, Hellums JD, Kroll MH, Turner NA, Moake JL (1995) Direct demonstration of radiolabeled von Willebrand factor binding to platelet glycoprotein Ib and IIb–IIIa in the presence of shear stress. Ann Biomed Eng 23:787CrossRefPubMed
32.
go back to reference Migliavacca F, Dubini G, Pennati G, Pietrabissa R, Fumero R, Hsia T-Y, de Leval MR (2000) Computational model of the fluid dynamics in systemic-to-pulmonary shunts. J Biomech 33:549–557CrossRefPubMed Migliavacca F, Dubini G, Pennati G, Pietrabissa R, Fumero R, Hsia T-Y, de Leval MR (2000) Computational model of the fluid dynamics in systemic-to-pulmonary shunts. J Biomech 33:549–557CrossRefPubMed
33.
go back to reference Miyazaki Y, Nomura S, Miyake T, Kagawa H, Kitada C, Taniguchi H, Komiyama Y, Fujimura Y, Ikeda Y, Fukuhara S (1996) High shear stress can initate both platelet aggregation and shedding of procoagulant containing microparticles. Blood 88:3456–3464PubMed Miyazaki Y, Nomura S, Miyake T, Kagawa H, Kitada C, Taniguchi H, Komiyama Y, Fujimura Y, Ikeda Y, Fukuhara S (1996) High shear stress can initate both platelet aggregation and shedding of procoagulant containing microparticles. Blood 88:3456–3464PubMed
34.
go back to reference Motz R, Wessel A, Ruschewski W, Bursch J (1999) Reduced frequency of occlusion of aorto-pulmonary shunts in infants receiving Aspirin. Cardiol Young. 9:474–477CrossRefPubMed Motz R, Wessel A, Ruschewski W, Bursch J (1999) Reduced frequency of occlusion of aorto-pulmonary shunts in infants receiving Aspirin. Cardiol Young. 9:474–477CrossRefPubMed
35.
go back to reference Mousa SA, Bennett JS (1996) Platelets in health and disease: platelet GPIIb/IIIa structure and function: recent advances in antiplatelet therapy. Drugs Future. 21:1141–1154 Mousa SA, Bennett JS (1996) Platelets in health and disease: platelet GPIIb/IIIa structure and function: recent advances in antiplatelet therapy. Drugs Future. 21:1141–1154
36.
go back to reference Moyle KR, Mallinson GD, Occleshaw CJ, Cowan BR, Gentles TL (2006) Wall shear stress is the primary mechanism of energy loss in the Fontan connection. Pediatr Cardiol 27:309–315CrossRefPubMed Moyle KR, Mallinson GD, Occleshaw CJ, Cowan BR, Gentles TL (2006) Wall shear stress is the primary mechanism of energy loss in the Fontan connection. Pediatr Cardiol 27:309–315CrossRefPubMed
37.
go back to reference Munson BR, Young DF, Okiishi TH (2002) Fundamentals of fluid mechanics, 4th edn. Wiley, New York, pp 350–352 Munson BR, Young DF, Okiishi TH (2002) Fundamentals of fluid mechanics, 4th edn. Wiley, New York, pp 350–352
38.
go back to reference Nakamura T, Uchiyama S, Yamazaki M, Iwata M (2002) Effects of dipyridamole and aspirin on shear-induced platelet aggregation in whole blood and platelet-rich plasma. Cerebrovasc Dis 14:234–238CrossRefPubMed Nakamura T, Uchiyama S, Yamazaki M, Iwata M (2002) Effects of dipyridamole and aspirin on shear-induced platelet aggregation in whole blood and platelet-rich plasma. Cerebrovasc Dis 14:234–238CrossRefPubMed
39.
go back to reference Nygard KK, Wilder M, Berkson J (1935) The relation between viscosity of the blood and the relative volume of erythrocytes (hematocrit value). Am. J Physiol 114:128–131 Nygard KK, Wilder M, Berkson J (1935) The relation between viscosity of the blood and the relative volume of erythrocytes (hematocrit value). Am. J Physiol 114:128–131
40.
go back to reference O’Brien JR (1990) Shear-induced platelet aggregation (Review Article). The Lancet. 335:711–713CrossRef O’Brien JR (1990) Shear-induced platelet aggregation (Review Article). The Lancet. 335:711–713CrossRef
41.
go back to reference Ohuchi H, Okabe H, Nagata N, Koseni K, Kaneko Y, Itoh K (1996) Long-term patency after the Blalock-Taussig operation-comparison between classic and modified shunts. Nihon Kyobugeka Gakkai Zasshi (J Jpn Assoc Thorac Surg) 44:1108–1113 Ohuchi H, Okabe H, Nagata N, Koseni K, Kaneko Y, Itoh K (1996) Long-term patency after the Blalock-Taussig operation-comparison between classic and modified shunts. Nihon Kyobugeka Gakkai Zasshi (J Jpn Assoc Thorac Surg) 44:1108–1113
42.
43.
go back to reference Ruggeri ZM, Orje JN, Haberman R, Federici AB, Reininger AJ (2006) Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108(6):1903–1910CrossRefPubMedCentralPubMed Ruggeri ZM, Orje JN, Haberman R, Federici AB, Reininger AJ (2006) Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108(6):1903–1910CrossRefPubMedCentralPubMed
44.
45.
go back to reference Shanmugavelayudam SK, Rubenstein DA, Yin W (2011) Effects of physiologically relevant dynamic shear stress on platelet complement activation. Platelets 22:602–610CrossRefPubMed Shanmugavelayudam SK, Rubenstein DA, Yin W (2011) Effects of physiologically relevant dynamic shear stress on platelet complement activation. Platelets 22:602–610CrossRefPubMed
46.
go back to reference Siggers JH, Waters SL (2005) Steady flows in pipes with finite curvature. Am Inst Phys Phys Fluids. 17(7):07102 Siggers JH, Waters SL (2005) Steady flows in pipes with finite curvature. Am Inst Phys Phys Fluids. 17(7):07102
47.
go back to reference Song M-H, Sato M, Ueda Y (2001) Three-dimensional simulation of the Blalock-Taussig shunt using computational fluid dynamics. Surg Today. 31:688–694CrossRefPubMed Song M-H, Sato M, Ueda Y (2001) Three-dimensional simulation of the Blalock-Taussig shunt using computational fluid dynamics. Surg Today. 31:688–694CrossRefPubMed
48.
go back to reference Takahashi M, Mason WH, Weiner K, McCurdy DK, Berdjis F, Peoples WM (2003) Changes in coronary artery aneurysms following treatment with Abciximab. Pediatr Res 53:164CrossRef Takahashi M, Mason WH, Weiner K, McCurdy DK, Berdjis F, Peoples WM (2003) Changes in coronary artery aneurysms following treatment with Abciximab. Pediatr Res 53:164CrossRef
49.
go back to reference Waniewski J, Kurowska W, Mizerski JK, Trykozko A, Nowinski K, Brzezinska-Rajszys G, Kosciesza A (2005) The effects of graft geometry on the patency of a systemic-to-pulmonary shunt: a computational fluid dynamics study. Artif Organs 29(8):642–650CrossRefPubMed Waniewski J, Kurowska W, Mizerski JK, Trykozko A, Nowinski K, Brzezinska-Rajszys G, Kosciesza A (2005) The effects of graft geometry on the patency of a systemic-to-pulmonary shunt: a computational fluid dynamics study. Artif Organs 29(8):642–650CrossRefPubMed
50.
go back to reference Wessel DL, Berger F, Li JS, Dahnert I, Rakhit A, Fontecave S, Newberger JW, for the CLARINET Investigators (2013) Clopidogrel in infants with systemic-to-pulmonary-artery shunts. N Engl J Med 368:2377–2384CrossRefPubMed Wessel DL, Berger F, Li JS, Dahnert I, Rakhit A, Fontecave S, Newberger JW, for the CLARINET Investigators (2013) Clopidogrel in infants with systemic-to-pulmonary-artery shunts. N Engl J Med 368:2377–2384CrossRefPubMed
51.
go back to reference Woolf PK, Stephenson LW, Meijboom E et al (1984) A comparison of Blalock-Taussig, Waterston, and polytetrafluoroethylene shunts in children less than two weeks of age. Ann Thorac Surg 38:26–30CrossRefPubMed Woolf PK, Stephenson LW, Meijboom E et al (1984) A comparison of Blalock-Taussig, Waterston, and polytetrafluoroethylene shunts in children less than two weeks of age. Ann Thorac Surg 38:26–30CrossRefPubMed
Metadata
Title
Computational Fluid Dynamics Characterization of Blood Flow in Central Aorta to Pulmonary Artery Connections: Importance of Shunt Angulation as a Determinant of Shear Stress-Induced Thrombosis
Authors
Carey Celestin
Martin Guillot
Nancy Ross-Ascuitto
Robert Ascuitto
Publication date
01-03-2015
Publisher
Springer US
Published in
Pediatric Cardiology / Issue 3/2015
Print ISSN: 0172-0643
Electronic ISSN: 1432-1971
DOI
https://doi.org/10.1007/s00246-014-1055-7

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