Abstract
The classical Fontan route, namely the atriopulmonary connection (APC), continues to be associated with a risk of thrombus formation in the atrium. A conversion to a total cavopulmonary connection (TCPC) from the APC can ameliorate hemodynamics for the failed Fontan; however, the impact of these surgical operations on thrombus formation remains elusive. This study elucidates the underlying mechanism of thrombus formation in the Fontan route by using a two-dimensional computer hemodynamic simulation based on a simple blood coagulation rule. Hemodynamics in the Fontan route was simulated with Navier–Stokes equations. The blood coagulation and the hemodynamics were combined using a particle method. Three models were created: APC with a square atrium, APC with a round atrium, and TCPC. To examine the effects of the venous blood flow velocity, the velocity at rest and during exercise (0.5 and 1.0 W/kg) was measured. The total area of the thrombi increased over time. The APC square model showed the highest incidence for thrombus formation, followed by the APC round, whereas no thrombus was formed in the TCPC model. Slower blood flow at rest was associated with a higher incidence of thrombus formation. The TCPC was superior to the classical APC in terms of preventing thrombus formation, due to significant blood flow stagnation in the atrium of the APC. Thus, local hemodynamic behavior associated with the complex channel geometry plays a major role in thrombus formation in the Fontan route.
Similar content being viewed by others
References
Balling G, Vogt M, Kaemmerer H et al (2000) Intracardiac thrombus formation after the Fontan operation. J Thorac Cardiovasc Surg 119:745–752. doi:10.1016/S0022-5223(00)70010-9
Cheung YF, Chay GW, Chiu CSW, Cheng LC (2005) Long-term anticoagulation therapy and thromboembolic complications after the Fontan procedure. Int J Cardiol 102:509–513. doi:10.1016/j.ijcard.2004.05.051
Coon PD (2001) Thrombus formation after the Fontan operation. Ann Thorac Surg 71:1990–1994
Efron B, Stein C (1981) The Jackknife estimate of variance. Ann Statist 9:586–596. doi:10.1214/aos/1176345462
Filipovic N, Kojic M, Tsuda A (2008) Modelling thrombosis using dissipative particle dynamics method. Philos Trans A Math Phys Eng Sci 366:3265–3279. doi:10.1098/rsta.2008.0097
Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248
Gewillig M, Brown SC, Eyskens B et al (2010) The Fontan circulation: who controls cardiac output? Interact Cardiovasc Thorac Surg 10:428–433. doi:10.1510/icvts.2009.218594
Giardini A, Napoleone CP, Specchia S et al (2006) Conversion of atriopulmonary Fontan to extracardiac total cavopulmonary connection improves cardiopulmonary function. Int J Cardiol 113:341–344. doi:10.1016/j.ijcard.2005.11.046
Hedrick M, Elkins RC, Knott-Craig CJ, Razook JD (1993) Successful thrombectomy for thrombosis of the right side of the heart after the Fontan operation. Report of two cases and review of the literature. J Thorac Cardiovasc Surg 105:297–301
Hjortdal VE (2003) Effects of exercise and respiration on blood flow in total cavopulmonary connection: a real-time magnetic resonance flow study. Circulation 108:1227–1231. doi:10.1161/01.CIR.0000087406.27922.6B
Jacobs ML, Pourmoghadam KK (2007) Thromboembolism and the role of anticoagulation in the Fontan patient. Pediatr Cardiol 28:457–464. doi:10.1007/s00246-007-9006-1
Jang WS, Kim WH, Choi K et al (2014) The mid-term surgical results of Fontan conversion with antiarrhythmia surgery. Eur J Cardiothorac Surg 45:922–927. doi:10.1093/ejcts/ezt511
Jin SM, Noh CI, Bae EJ et al (2007) Impaired vascular function in patients with Fontan circulation. Int J Cardiol 120:221–226. doi:10.1016/j.ijcard.2006.09.020
Kamada H, Tsubota K, Nakamura M et al (2010) A three-dimensional particle simulation of the formation and collapse of a primary thrombus. Int J Numer Meth Biomed Eng 26:488–500. doi:10.1002/cnm.1367
Koshizuka S, Nobe A, Oka Y (1998) Numerical analysis of breaking waves using the moving particle semi-implicit method. Int J Numer Meth Fluids 26:751–769. doi:10.1002/(SICI)1097-0363(19980415)26:7<751:AID-FLD671>3.0.CO;2-C
Lardo AC, Del Nido PJ, Webber SA et al (1997) Hemodynamic effect of progressive right atrial dilatation in atriopulmonary connections. J Thorac Cardiovasc Surg 114:2–8. doi:10.1016/S0022-5223(97)70110-7
Lardo AC, Webber SA, Friehs I et al (1999) Fluid dynamic comparison of intra-atrial and extracardiac total cavopulmonary connections. J Thorac Cardiovasc Surg 117:697–704. doi:10.1016/S0022-5223(99)70289-8
Liang F, Sughimoto K, Matsuo K et al (2014) Patient-specific assessment of cardiovascular function by combination of clinical data and computational model with applications to patients undergoing Fontan operation. Int J Numer Meth Biomed Eng 30:1000–1018. doi:10.1002/cnm.2641
Mahle WT, Todd K, Fyfe DA (2003) Endothelial function following the Fontan operation. Am J Cardiol 91:1286–1288. doi:10.1016/S0002-9149(03)00289-3
Mavroudis C, Backer CL, Deal BJ et al (2001) Total cavopulmonary conversion and maze procedure for patients with failure of the Fontan operation. J Thorac Cardiovasc Surg 122:863–871. doi:10.1067/mtc.2001.117840
McCrindle BW, Manlhiot C, Cochrane A et al (2013) Factors associated with thrombotic complications after the Fontan procedure. J Am Coll Cardiol 61:346–353. doi:10.1016/j.jacc.2012.08.1023
Monagle P, Cochrane A, Roberts R et al (2011) A multicenter, randomized trial comparing heparin/warfarin and acetylsalicylic acid as primary thromboprophylaxis for 2 years after the Fontan procedure in children. J Am Coll Cardiol 58:645–651. doi:10.1016/j.jacc.2011.01.061
Odegard KC, Zurakowski D, DiNardo JA et al (2009) Prospective longitudinal study of coagulation profiles in children with hypoplastic left heart syndrome from stage I through Fontan completion. J Thorac Cardiovasc Surg 137:934–941. doi:10.1016/j.jtcvs.2008.09.031
Rychik J (2010) Forty years of the Fontan operation: a failed strategy. YPCSU 13:96–100. doi:10.1053/j.pcsu.2010.02.006
Sheikh AM, Tang ATM, Roman K et al (2004) The failing Fontan circulation: successful conversion of atriopulmonary connections. J Thorac Cardiovasc Surg 128:60–66. doi:10.1016/j.jtcvs.2004.02.011
Tamagawa M, Kaneda H, Hiramoto M, Nagahama S (2009) Simulation of thrombus formation in shear flows using lattice Boltzmann method. Artif Organs 33:604–610. doi:10.1111/j.1525-1594.2009.00782.x
Tomkiewicz-Pajak L, Hoffman P, Trojnarska O et al (2014) Abnormalities in blood coagulation, fibrinolysis, and platelet activation in adult patients after the Fontan procedure. J Thorac Cardiovasc Surg 147:1284–1290. doi:10.1016/j.jtcvs.2013.06.011
Tsubota K, Wada S (2010) Effect of the natural state of an elastic cellular membrane on tank-treading and tumbling motions of a single red blood cell. Phys Rev E: Stat Nonlin Soft Matter Phys 81:011910. doi:10.1103/PhysRevE.81.011910
Tsubota K, Wada S, Yamaguchi T (2006) Particle method for computer simulation of red blood cell motion in blood flow. Comput Methods Programs Biomed 83:139–146. doi:10.1016/j.cmpb.2006.06.005
van Son JA, Mohr FW, Hambsch J et al (1999) Conversion of atriopulmonary or lateral atrial tunnel cavopulmonary anastomosis to extracardiac conduit Fontan modification. Eur J Cardiothorac Surg 15:150–157
Weinstein S, Chan D (2005) Extracardiac Fontan conversion, cryoablation, and pacemaker placement for patients with a failed Fontan. Semin Thorac Cardiovasc Surg 17:170–178. doi:10.1053/j.semtcvs.2005.02.007
Wolberg AS, Aleman MM, Leiderman K, Machlus KR (2012) Procoagulant activity in hemostasis and thrombosis: Virchow’s triad revisited. Anesth Analg 114:275–285. doi:10.1213/ANE.0b013e31823a088c
Acknowledgments
This study was partially supported by the Inohana Alumni Association of the Chiba University of Medicine (12046) and a research grant, JSPS (25630046).
Conflict of interest
There is no conflict of interest to declare.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sughimoto, K., Okauchi, K., Zannino, D. et al. Total Cavopulmonary Connection is Superior to Atriopulmonary Connection Fontan in Preventing Thrombus Formation: Computer Simulation of Flow-Related Blood Coagulation. Pediatr Cardiol 36, 1436–1441 (2015). https://doi.org/10.1007/s00246-015-1180-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00246-015-1180-y