Hemodynamic performance of the fontan circulation compared with a normal biventricular circulation: A computational model study

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 7, 2014, Pages H1056-H1072

  Liang, Fuyou ^a   Senzaki, Hideaki ^b   Kurishima, Clara ^b   Sughimoto, Koichi ^c   Inuzuka, Ryo ^d   Liu, Hao ^a,e  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SAITAMA MEDICAL UNIVERSITY   (Japan)

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

^d UNIVERSITY OF TOKYO   (Japan)

^e CHIBA UNIVERSITY   (Japan)

Author keywords

Cardiac output; Cardiovascular properties; Central venous pressure; Computational model; Fontan circulation

Indexed keywords

ARTICLE; ASSISTED CIRCULATION; BLOOD VESSEL COMPLIANCE; CARDIOVASCULAR SYSTEM; EXTRACORPOREAL CIRCULATION; FONTAN CIRCULATION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE FILLING PRESSURE; HEART RATE; HEART VENTRICLE CONTRACTILITY; HEMODYNAMIC PARAMETERS; INTERMETHOD COMPARISON; LUNG VASCULAR RESISTANCE; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; SYSTEMIC VASCULAR RESISTANCE; BIOLOGICAL MODEL; CORONARY ARTERY BLOOD FLOW; FONTAN PROCEDURE; HEMODYNAMICS; HUMAN;

CORONARY CIRCULATION; FONTAN PROCEDURE; HEMODYNAMICS; HUMANS; MODELS, CARDIOVASCULAR;

EID: 84907674609     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00245.2014     Document Type: Article

References (94)

1. Ahnve S, Vallin H. Influence of heart rate and inhibition of autonomic tone on the QT interval. Circulation 65: 435–439, 1982.
2. Alexi-Meskishvili V, Ovroutski S, Ewert P, Dähnert I, Berger F, Lange PE, Hetzer R. Optimal conduit size for extracardiac Fontan operation. Eur J Cardiothorac Surg 18: 690–695, 2000.
3. Ando M, Takahashi Y. Long-term functional analysis of the atrioventricular valve in patients undergoing single ventricle palliation. Ann Thorac Surg 92: 1767–1773, 2011.
4. Arbab-Zadeh A, Dijk E, Prasad A, Fu Q, Torres P, Zhang R, Thomas JD, Palmer D, Levine BD. Effect of aging and physical activity on left ventricular compliance. Circulation 110: 1799–1805, 2004.
5. Aune E, Baekkevar M, Roislien J, Rodevand O, Otterstad JE. Normal reference ranges for left and right atrial olume indexes and ejection fractions obtained with real-time three-dimensional echocardiography. Eur J Echocardiogr 10: 738–744, 2009.
6. Barber G, Di Sessa T, Child JS, Perloff JK, Laks H, George BL, Williams RG. Hemodynamic responses to isolated increments in heart rate by atrial pacing after a Fontan procedure. Am Heart J 115: 837–841, 1988.
7. Bedotto JB, Grayburn PA, Black WH, Raya TE, McBride W, Hsia HH, Eichhorn EJ. Alterations in left ventricular relaxation during atrioventricular pacing in humans. J Am Coll Cardiol 15: 658–664, 1990.
8. Benatar A, Decraene T. Comparison of formulae for heart rate correction of QT interval in exercise ECGs from healthy children. Heart 86: 199–202, 2001.
9. Border WL, Syed AU, Michelfelder EC, Khoury P, Uzark KC, Manning PB, Pearl JM. Impaired systemic ventricular relaxation affects postoperative short-term outcome in Fontan patients. J Thorac Cardiovasc Surg 126: 1760–1764, 2003.
10. Braunwald E, Moscovitz HL, Amram SS, Lasser RP, Sapin SO, Himmelstein A, Ravitch MM, Gordon AJ. The hemodynamics of the left side of the heart as studied by simultaneous left atrial, left ventricular, and aortic pressures; particular reference to mitral stenosis. Circulation 12: 69–81, 1955.
11. Braunwald E, Brockenbrough EC, Frahm CJ, Ross J Jr. Left atrial and left ventricular pressures in subjects without cardiovascular disease: observations in eighteen patients studied by transseptal left heart catheterization. Circulation 24: 267–269, 1961.
12. Brody JS, Stemmler EJ, DuBois AB. Longitudinal distribution of vascular resistance in the pulmonary arteries, capillaries, and veins. J Clin Invest 47: 783–99, 1968.
13. Calvin JE, Driedger AA, Sibbald WJ. The hemodynamic effect of rapid fluid infusion in critically ill patients. Surgery 90: 61–76, 1981.
14. Cheung YF, Penny DJ, Redington AN. Serial assessment of left ventricular diastolic function after Fontan procedure. Heart 83: 420–424, 2000.
15. Davey P. A new physiological method for heart rate correction of the QT interval. Heart 82: 183–186, 1999.
16. de Leval MR. The Fontan circulation: a challenge to William Harvey? Nat Clin Pract Cardiovasc Med 2: 202–208, 2005.
17. de Leval M., Deanfield JE. Four decades of Fontan palliation. Nat Rev Cardiol 7: 520–527, 2010.
18. Dexter L, Dow JW, Haynes FW, Whittenberger JL, Ferris BG, Goodale WT, Hellems HK. Studies of the pulmonary circulation in man at rest; normal variations and the interrelations between increased pulmonary blood flow, elevated pulmonary arterial pressure, and high pulmonary “capillary” pressures. J Clin Invest 29: 602–613, 1950.
19. Ding J, Liu Y, Wang F. Influence of bypass angles on extracardiac Fontan connections: a numerical study. Int J Numer Method Biomed Eng 29: 351–362, 2013.
20. Dogan A, Tunc E, Varol E, Ozaydin M, Ozturk M. Comparison of the four formulas of adjusting QT interval for the heart rate in the middle-aged healthy Turkish men. Ann Noninvasive Electrocardiol 10: 134–141, 2005.
21. Fioretti P, Brower RW, Meester GT, Serruys PW. Interaction of left ventricular relaxation and filling during early diastole in human subjects. Am J Cardiol 46: 197–203, 1980.
22. Fowler NO, Westcott RN, Scott RC. Normal pressure in the right heart and pulmonary artery. Am Heart J 46: 264–267, 1953.
23. Frommelt PC, Snider AR, Meliones JN, Vermilion RP. Doppler assessment of pulmonary artery flow patterns and ventricular function after the Fontan operation. Am J Cardiol 68: 1211–1215, 1991.
24. Garcia D, Barenbrug PJ, Pibarot P, Dekker AL, van der Veen FH, Maessen JG, Dumesnil JG, Durand LG. A ventricular-vascular coupling model in presence of aortic stenosis. Am J Physiol Heart Circ Physiol 288: H1874–H1884, 2005.
25. Garofalo CA, Cabreriza SE, Quinn TA, Weinberg AD, Printz BF, Hsu DT, Quaegebeur JM, Mosca RS, Spotnitz HM. Ventricular diastolic stiffness predicts perioperative morbidity and duration of pleural effusions after the Fontan operation. Circulation 114, Suppl 1: I56–I61, 2006.
26. Gewillig M., Lundström UR, Bull C, Wyse RK, Deanfield JE. Exercise responses in patients with congenital heart disease after Fontan repair: patterns and determinants of performance. J Am Coll Cardiol 15: 1424–1432, 1990.
27. Gewillig M, Wyse RK, de Leval M., Deanfield JE. Early and late arrhythmias after the Fontan operation: predisposing factors and clinical consequences. Br Heart J 67: 72–79, 1992.
28. Gewillig M, Brown SC, Eyskens B, Heying R, Ganame J, Budts W, La Gerche A, Gorenflo M. The Fontan circulation: who controls cardiac output? Interact Cardiovasc Thorac Surg 10: 428–433, 2010.
29. Goldberg DJ, French B, Szwast AL, McBride MG, Marino BS, Mirarchi N, Hanna BD, Wernovsky G, Paridon SM, Rychik J. Impact of sildenafil on echocardiographic indices of myocardial performance after the Fontan operation. Pediatr Cardiol 33: 689–696, 2012.
30. Hager A, Fratz S, Schwaiger M, Lange R, Hess J, Stern H. Pulmonary blood flow patterns in patients with Fontan circulation. Ann Thorac Surg 85: 186–191, 2008.
31. Haggerty CM, Kanter KR, Restrepo M, de Zélicourt DA, Parks WJ, Rossignac J, Fogel MA, Yoganathan AP. Simulating hemodynamics of the Fontan Y-graft based on patient-specific in vivo connections. J Thorac Cardiovasc Surg 145: 663–670, 2013.
32. Harrison DA, Liu P, Walters JE, Goodman JM, Siu SC, Webb GD, Williams WG, McLaughlin PR. Cardiopulmonary function in adult patients late after Fontan repair. J Am Coll Cardiol 26: 1016–1021, 1995.
33. Heldt T, Shim EB, Kamm RD, Mark RG. Computational modeling of cardiovascular response to orthostatic stress. J Appl Physiol 92: 1239–1254, 2002.
34. Houlind K, Stenbøg EV, Sørensen KE, Emmertsen K, Hansen OK, Rybro L, Hjortdal VE. Pulmonary and caval flow dynamics after total cavopulmonary connection. Heart 81: 67–72, 1999.
35. Hsia TY, Migliavacca F, Pittaccio S, Radaelli A, Dubini G, Pennati G, de Leval M. Computational fluid dynamic study of flow optimization in realistic models of the total cavopulmonary connections. J Surg Res 116: 305–313, 2004.
36. Karjalainen J, Viitasalo M, Mänttäri M, Manninen V. Relation between QT intervals and heart rates from 40 to 120 beats/min in rest electrocardiograms of men and a simple method to adjust QT interval values. J Am Coll Cardiol 23: 1547–1553, 1994.
37. Kouatli AA, Garcia JA, Zellers TM, Weinstein EM, Mahony L. Enalapril does not enhance exercise capacity in patients after Fontan procedure. Circulation 96: 1507–1512, 1997.
38. Krishnan US, Taneja I, Gewitz M, Young R, Stewart J. Peripheral vascular adaptation and orthostatic tolerance in Fontan physiology. Circulation 120: 1775–1783, 2009.
39. Kung E, Baretta A, Baker C, Arbia G, Biglino G, Corsini C, Schievano S, Vignon-Clementel IE, Dubini G, Pennati G, Taylor A, Dorfman A, Hlavacek AM, Marsden AL, Hsia TY, Migliavacca F; Modeling Of Congenital Hearts Alliance (MOCHA) Investigators. Predictive modeling of the virtual Hemi-Fontan operation for second stage single ventricle palliation: two patient-specific cases. J Biomech 46: 423–429, 2013.
40. Kung E, Pennati G, Migliavacca F, Hsia TY, Figliola RS, Marsden A, Giardini A. A simulation protocol for exercise physiology in Fontan patients using a closed-loop lumped-parameter model. J Biomech Eng 2014 Aug. [Epub ahead of print].
41. La Gerche A, Gewillig M. What limits cardiac performance during exercise in normal subjects and in healthy Fontan patients? Int J Pediatr 2010: 791291.
42. Lambert E, d’Udekem Y, Cheung M, Sari CI, Inman J, Ahimastos A, Eikelis N, Pathak A, King I, Grigg L, Schlaich M, Lambert G. Sympathetic and vascular dysfunction in adult patients with Fontan circulation. Int J Cardiol 167: 1333–1338, 2013.
43. Lee KJ, Yoo SJ, Holtby H, Grant B, Mroczek D, Wong D, Grosse-Wortmann L, Benson LN, Chaturvedi RR. Acute effects of the ACE inhibitor enalaprilat on the pulmonary, cerebral and systemic blood flow and resistance after the bidirectional cavopulmonary connection. Heart 97: 1343–1348, 2011.
44. Liang FY, Liu H. Simulation of hemodynamic responses to the Valsalva maneuver: an integrative computational model of the cardiovascular system and the autonomic nervous system. J Physiol Sci 56: 45–65, 2006.
45. Liang F, Sughimoto K, Matsuo K, Liu H, Takagi S. Patient-specific assessment of cardiovascular function by combination of clinical data and computational model with applications to patients undergoing Fontan operation. Int J Numer Method Biomed Eng 2014 Apr 21. [Epub ahead of print].
46. Liang F, Takagi S, Himeno R, Liu H. Multi-scale modeling of the human cardiovascular system with applications to aortic valvular and arterial stenoses. Med Biol Eng Comput 47: 743–755, 2009.
47. Liu CP, Ting CT, Lawrence W, Maughan WL, Chang MS, Kass DA. Diminished contractile response to increased heart rate in intact human left ventricular hypertrophy. Systolic versus diastolic determinants. Circulation 88: 1893–1906, 1993.
48. Macé L, Dervanian P, Bourriez A, Mazmanian GM, Lambert V, Losay J, Neveux JY. Changes in venous return parameters associated with univentricular Fontan circulations. Am J Physiol Heart Circ Physiol 279: H2335–H23343, 2000.
49. Magder S, Bafaqeeh F. The clinical role of central venous pressure measurements. J Intensive Care Med 22: 44–51, 2007.
50. Magosso E, Cavalcanti S, Ursino M. Theoretical analysis of rest and exercise hemodynamics in patients with total cavopulmonary connection. Am J Physiol Heart Circ Physiol 282: H1018–H1034, 2002.
51. McEniery CM, Yasmin Hall IR, Qasem A, Wilkinson IB, Cockcroft JR; ACCT Investigators. Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol 46: 1753–1760, 2005.
52. Miera O, Potapov EV, Berger F. End-stage heart failure in children or patients suffering from congenital heart disease: are new treatment options emerging? Eur J Cardiothorac Surg 43: 886–887, 2013.
53. Migliavacca F, Balossino R, Pennati G, Dubini G, Hsia TY, de Leval M., Bove EL. Multiscale modelling in biofluidynamics: application to reconstructive paediatric cardiac surgery. J Biomech 39: 1010–1020, 2006.
54. Milnor WR, Jose AD, Mcgaff CJ. Pulmonary vascular volume, resistance, and compliance in man. Circulation 22: 130–137, 1960.
55. Moghadam ME, Vignon-Clementel IE, Figliola R, Marsden AL; Modeling of Congenital Hearts Alliance (MOCHA) Investigators. A modular numerical method for implicit 0D/3D coupling in cardiovascular finite element simulations. J Comput Physics 244: 63–79, 2013.
56. Mondésert B, Marcotte F, Mongeon FP, Dore A, Mercier LA, Ibrahim R, Asgar A, Miro J, Poirier N, Khairy P. Fontan circulation: success or failure? Can J Cardiol 29: 811–820, 2013.
57. Naito Y, Hiramatsu T, Kurosawa H, Agematsu K, Sasoh M, Nakanishi T, Imai Y, Yamazaki K. Long-term results of modified fontan operation for single-ventricle patients associated with atrioventricular valve regurgitation. Ann Thorac Surg 96: 211–218, 2013.
58. Ohuchi H, Miyazaki A, Watanabe T, Yamada O, Yagihara T, Echigo S. Hemodynamic deterioration during simulated supraventricular tachycardia in patients after the Fontan operation. Int J Cardiol 117: 381–387, 2007.
59. Ohuchi H, Yasuda K, Miyazaki A, Kitano M, Sakaguchi H, Yazaki S, Tsuda E, Yamada O. Haemodynamic characteristics before and after the onset of protein losing enteropathy in patients after the Fontan operation. Eur J Cardiothorac Surg 43: e49–e57, 2013.
60. Olufsen MS, Ottesen JT, Tran HT, Ellwein LM, Lipsitz LA, Novak V. Blood pressure and blood flow variation during postural change from sitting to standing: model development and validation. J Appl Physiol 99: 1523–1537, 2005.
61. Piran S, Veldtman G, Siu S, Webb GD, Liu PP. Heart failure and ventricular dysfunction in patients with single or systemic right ventricles. Circulation 105: 1189–1194, 2002.
62. Paridon SM, Mitchell PD, Colan SD, Williams RV, Blaufox A, Li JS, Margossian R, Mital S, Russell J, Rhodes J; Pediatric Heart Network Investigators. A cross-sectional study of exercise performance during the first 2 decades of life after the Fontan operation. J Am Coll Cardiol 52: 99–107, 2008.
63. Pennati G, Corsini C, Cosentino D, Hsia TY, Luisi VS, Dubini G, Migliavacca F. Boundary conditions of atient-specific fluid dynamics modelling of cavopulmonary connections: possible adaptation of pulmonary resistances results in a critical issue for a virtual surgical planning. Interface Focus 1: 297–307, 2011.
64. Pennati G, Migliavacca F, Dubini G, Pietrabissa R, de Leval MR. A mathematical model of circulation in the presence of the bidirectional cavopulmonary anastomosis in children with a univentricular heart. Med Eng Phys 19: 223–234, 1997.
65. Pennati G, Corsini C, Hsia TY, Migliavacca F; Modeling of Congenital Hearts Alliance (MOCHA) Investigators. Computational fluid dynamics models and congenital heart diseases. Front Pediatr 1: 4. eCollection, 2013.
66. Penny DJ, Rigby ML, Redington AN. Abnormal patterns of intraventricular flow and diastolic filling after the Fontan operation: evidence for incoordinate ventricular wall motion. Br Heart J 66: 375–378, 1991.
67. Presson RG Jr, Audi SH, Hanger CC, Zenk GM, Sidner RA, Linehan JH, Wagner WW Jr, Dawson CA. Anatomic distribution of pulmonary vascular compliance. J Appl Physiol 84: 303–310, 1998.
68. Redington A. The physiology of the Fontan circulation. Progr Pediatr Cardiol 22: 179–186, 2006.
69. Rickards AF, Norman J. Relation between QT interval and heart rate. New design of physiologically adaptive cardiac pacemaker. Br Heart J 45: 56–61, 1981.
70. Sagie A, Larson MG, Goldberg RJ, Bengtson JR, Levy D. An improved method for adjusting the QT interval for heart rate (the Framingham Heart Study). Am J Cardiol 70: 797–801, 1992.
71. Salton CJ, Chuang ML, O’Donnell CJ, Kupka MJ, Larson MG, Kissinger KV, Edelman RR, Levy D, Manning WJ. Gender differences and normal left ventricular anatomy in an adult population free of hypertension. A cardiovascular magnetic resonance study of the Framingham Heart Study Offspring cohort. J Am Coll Cardiol 39: 1055–1060, 2002.
72. Scharhag J, Schneider G, Urhausen A, Rochette V, Kramann B, Kindermann W. Athlete’s heart: right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging. J Am Coll Cardiol 40: 1856–1863, 2002.
73. Schlant RC, Sonnenblick EH, Katz AM. Normal physiology of the cardiovascular system. In: Hurst’s The Heart (9th ed.). New York McGraw-Hill, 1998, vol. 3, p. 113–115.
74. Senzaki H, Chen CH, Kass DA. Single-beat estimation of end-systolic pressure-volume relation in humans. A new method with the potential for noninvasive application. Circulation 94: 2497–2506, 1996.
75. Senzaki H, Isoda T, Ishizawa A, Hishi T. Reconsideration of criteria for the Fontan operation. Influence of pulmonary artery size on postoperative hemodynamics of the Fontan operation. Circulation 89: 1196–1202, 1994.
76. Senzaki H, Masutani S, Ishido H, Taketazu M, Kobayashi T, Sasaki N, Asano H, Katogi T, Kyo S, Yokote Y. Cardiac rest and reserve function in patients with Fontan circulation. J Am Coll Cardiol 47: 2528–2535, 2006.
77. Shi Y, Lawford P, Hose R. Review of zero-D and 1-D models of blood flow in the cardiovascular system. Biomed Eng Online 10: 33, 2011.
78. Sorensen GK, Ramamoorthy C, Lynn AM, French J, Stevenson JG. Hemodynamic effects of amrinone in children after Fontan surgery. Anesth Analg 82: 241–246, 1996.
79. Starling MR, Montgomery DG, Mancini GB, Walsh RA. Load independence of the rate of isovolumic relaxation in man. Circulation 76: 1274–1281, 1987.
80. Stead EA, Warren JV, Merrill AJ, Brannon ES. The cardiac output in male subjects as measured by the technique of right atrial catheterization. Normal values with observations on the effect of anxiety and tilting. J Clin Invest 24: 326–331, 1945.
81. Suga H, Sagawa K, Shoukas AA. Load independence of the instantaneous pressure-volume ratio of the canine left ventricle and effects of epinephrine and heart rate on the ratio. Circ Res 32: 314–322, 1973.
82. Sughimoto K, Liang F, Takahara Y, Mogi K, Yamazaki K, Takagi S, Liu H. Assessment of cardiovascular function by combining clinical data with a computational model of the cardiovascular system. J Thorac Cardiovasc Surg 145: 1367–1372, 2013.
83. Sun Q, Liu J, Qian Y, Zhang H, Wang Q, Sun Y, Hong H, Liu J. Computational haemodynamic analysis of patient-specific virtual operations for total cavopulmonary connection with dual superior venae cavae. Eur J Cardiothorac Surg 45: 564–569, 2014.
84. Sun Y, Beshara M, Lucariello RJ, Chiaramida SA. A comprehensive model for right-left heart interaction under the influence of pericardium and baroreflex. Am J Physiol Heart Circ Physiol 272: H1499–H1515, 1997.
85. Sundareswaran KS, Pekkan K, Dasi LP, Whitehead K, Sharma S, Kanter KR, Fogel MA, Yoganathan AP. The total cavopulmonary connection resistance: a significant impact on single ventricle hemodynamics at rest and exercise. Am J Physiol Heart Circ Physiol 295: H2427–H2435, 2008.
86. Szabó G, Buhmann V, Graf A, Melnitschuk S, Bährle S, Vahl CF, Hagl S. Ventricular energetics after the Fontan operation: contractilityafterload mismatch. J Thorac Cardiovasc Surg 125: 1061–1069, 2003.
87. Troianowski G, Taylor CA, Feinstein JA, Vignon-Clementel IE. Three-dimensional simulations in Glenn patients: clinically based boundary conditions, hemodynamic results and sensitivity to input data. J Biomech Eng 133: 111006, 2011.
88. Uemura H, Yagihara T, Kawashima Y, Yamamoto F, Nishigaki K, Matsuki O, Okada K, Kamiya T, Anderson RH. What factors affect ventricular performance after a Fontan-type operation? J Thorac Cardiovasc Surg 110: 405–415, 1995.
89. Van Griensven A, Meixner T, Grunwald S, Bishop T, Diluzio M, Srinivasan R. A global sensitivity analysis tool for the parameters of multi-variable catchment models. J Hydrol 324: 10–23, 2006.
90. van Heusden K, Gisolf J, Stok WJ, Dijkstra S, Karemaker JM. Mathematical modeling of gravitational effects on the circulation: importance of the time course of venous pooling and blood volume changes in the lungs. Am J Physiol Heart Circ Physiol 291: H2152–H2165, 2006.
91. Voges I, Jerosch-Herold M, Hart C, Scheewe J, Gabbert DD, Pardun E, Kramer HH, Rickers C. Anatomical and functional assessment of the intra-atrial lateral tunnel in the Fontan circulation. Eur J Cardiothorac Surg 44: 462–467, 2013.
92. Wang Y, Gutman JM, Heilbron D, Wahr D, Schiller NB. Atrial volume in a normal adult population by two-dimensional echocardiography. Chest 86: 595–601, 1984.
93. Williams DB, Kiernan PD, Schaff HV, Marsh HM, Danielson GK. The hemodynamic response to dopamine and nitroprusside following right atrium-pulmonary artery bypass (Fontan procedure). Ann Thorac Surg 34: 51–57, 1982.
94. Yamaguchi K, Tanabe K, Tani T, Yagi T, Fujii Y, Konda T, Kawai J, Sumida T, Morioka S, Kihara Y. Left atrial volume in normal Japanese adults. Circ J 70: 285–288, 2006.