The pathophysiology and complications of Fontan circulation
Keywords:
Fontan, Pathophisiology, Complications, Univentricular heartAbstract
The Fontan operation has been the final palliation for patients born with congenital heart defects with a functional single ventricle for more than 4 decades. The “normal” Fontan physiology is characterized by the loss of the sub-pulmonary ventricle with consequent elevated pressure in the caval system, non-pulsatile blood flow in the pulmonary circulation and at least mild reduction of the systemic output. When successful, this procedure is associated with a range of benefits including improved arterial saturation and abolishment of chronic volume overload, allowing a fairly normal life to the majority of patients through early adulthood. As we enter the 5th decade of caring for patients palliated with the Fontan procedure, it is evident that adult survivors face significant morbidity due to multiorgan dysfunction, early mortality and need for heart transplantation. Several late complications may occur: ventricular dysfunction, arrhythmia, cyanosis, exercise intolerance, elevated pulmonary vascular resistance, protein-losing enteropathy, plastic bronchitis, hepatic and renal complications. The mechanism of late Fontan failure is multifactorial and not completely understood, it depends on interactions between the ventricle, the pulmonary vascular bed, the venous and lymphatic compartments.
Conclusions: the aim of this review is to describe the pathophysiology of Fontan circulation and the clinical and hemodynamic characteristics of early and late failing Fontan survivors, their association with morbidity and mortality, and the strategies for their management.
References
1. Fontan F and Baudet E. Surgical repair of tricuspid atresia. Thorax 1971;26:240-248.
2. Glenn WW, Circulatory by-pass of the right side of the heart - shunt between the superior vena cava and distal right pulmonary artery - report of a clinical application. N Engl J Med 1958;259:117-120.
3. Kreutzer G, Schlichter A, Laura JP, Suàrez JC, Vargas JF. Univentricular heart with low pulmonary vascular resistances: septation vs. atriopulmonary anastomosis. Arq Bras Cardiol 1981;37:301–307.
4. Björk V, Olin C, Bjarke B, Thore C. Right atrial-right ventricular anastomosis for correction of tricuspid atresia. J Thorac Cardiovasc Surg 1979;77:452–458.
5. De Leval M, Kilner P, Gewillig M, Bull C. Total cavo-pulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. Experimental studies and early clinical experience. J Thorac Cardiovasc Surg 1988;96:682-695.
6. Puga FJ, Chavareli M, Hagler DJ. Modification of the Fontan operation applicable to the patients with left atriovascular valve. Circulation 1987;76:11153–11160.
7. Marcelletti C, Corno A, Giannico S, Marino B. Inferior vena cava - pulmonary artery extracardiac conduit. A new form of right heart bypass. J Thorac Cardiovasc Surg 1990;100:228–232.
8. Gewillig M, Brown S. The Fontan circulation after 45 years: update in physiology. Heart 2016;102:1081–1086.
9. Rychik J, Fogel MA, Donofrio MT, Goldmuntz E, Cohen MS, Spray TL, Jacobs ML. Comparison of patterns of pulmonary venous blood flow in the functional single ventricle heart after operative aortopulmonary shunt versus superior cavopulmonary shunt. Am J Cardiol 1997;80:922-926.
10. Veldtman GR, Opotowsky AR, Wittekind SG, Rychik J, Penny DJ, Fogel M, Marino BS, Gewillig M. Cardiovascular adaptation to the Fontan circulation. Congenit Heart Dis 2017;12:699-710.
11. 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 2010;10:428-433.
12. Claessen G, La Gerche A, Van De Bruaene A, Claeys M, Willems R, Dymarkowski S, Bogaert J, Claus P, Budts W, Heidbuchel H, Gewillig M. Heart Rate Reserve in Fontan Patients: Chronotropic Incompetence or hemodynamic Limitation? J Am Heart Assoc 2019;8:e012008.
13. Kreutzer C, Kreutzer J, Kreutzer GO. Reflections on five decades of the Fontan Kreutzer procedure. Front Pediatr 2013;1:45.
14. Haworth SG, Reid L. Quantitative structural study of pulmonary circulation in the new-born with aortic atresia, stenosis, or coarctation. Thorax 1977;32:121-128.
15. Gewillig M, Brownb SC, Heyinga R, Eyskensa B, Ganamea J, Boshoffa DE, Budts W, Gorenflo M. Volume load paradox while preparing for the Fontan: not too much for the ventricle, not too little for the lungs. Interact Cardiovasc Thorac Surg 2010;10:262–265.
16. Khairy P, Fernandes SM, Mayer JE, Triedman JK, Walsh EP, Lock JE, Landzberg MJ. Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 2008;117:85–92.
17. Henaine R, Vergnat M, Bacha EA, Baudet B, Lambert V, Belli E, Serraf A. Effects of lack of pulsatility on pulmonary endothelial function in the Fontan circulation. J Thorac Cardiovasc Surg 2013;146:522-529.
18. Khambadkone S, Li J, De Leval MR, Cullen S, Deanfield JE, Redington AN. Basal pulmonary vascular resistance and nitric oxide responsiveness late after Fontan-type operation. Circulation 2003;107:3204-3208.
19. Hiramatsu T, Imai Y, Takanashi Y, Seo K, Terada M, Aoki M, Nakazawa M. Time Course of Endothelin-1 and Adrenomedullin After the Fontan Procedure. Ann Thorac Surg 1999;68:169–172.
20. Agnoletti G, Gala S, Ferroni F, Bordese R, Appendini L, Pace Napoleone C, Bergamasco L. Endothelin inhibitors lower pulmonary vascular resistance and improve functional capacity in patients with Fontan circulation. J Thorac Cardiovasc Surg 2017;153:1468-1475.
21. Alsaied T, Sleeper LA, Masci M, Ghelani SJ, Azcue N, Geva T, Powell AJ and Rathod RH. Maldistribution of pulmonary blood flow in patients after the Fontan operation is associated with worse exercise capacity. J Cardiovasc Magn Reson 2018;20:85.
22. Erikssen G, Aboulhosn J, Lin J, Liestøl K, Estensen ME, Gjesdal O, Skulstad H, Døhlen G, Lindberg HL. Survival in patients with univentricular hearts: the impact of right versus left ventricular morphology. Open Heart 2018;5:e000902.
23. Lastinger L, Zaidi AN. The adult with a Fontan: a panacea without a cure? Review of long-term complications. Circ J 2013;77:2672–2681.
24. Whitehead K, Gillespie MJ, Harris MA, Fogel MA, and Rome JJ. Noninvasive Quantification of Systemic To Pulmonary Collateral Flow: A Major Source of Inefficiency in Patients with Superior Cavopulmonary Connections. Circ Cardiovasc Imaging 2009;2:405–411.
25. Downing TE, Allen KY, Goldberg DJ, Rogers LS, Ravishankar C, Rychik J, Fuller S, Montenegro LM, Steven JM, Gillesple MJ, Rome JJ, Spray TL, Nicolson SC, Gaynor LW, Glatz AC. Surgical and Catheter-Based Reinterventions Are Common in Long-Term Survivors of the Fontan Operation. Circ Cardiovasc Interv 2017;10:e004924.
26. Buendìa-Fuentes F, Melero-Ferrer JL, Plaza-Lòpez D, Rueda-Soriano J, Osa-Saez A, Aguero J, Calvillo-Batllés P. Fonfria-Esparcia C, Ballesta-cunat A, Marti-Bonmati L, Martinez-Dolz L. Noninvasive Liver Assessment in Adult Patients With Fontan Circulation Using Acoustic Radiation Force Impulse Elastography and Hepatic Magnetic Resonance Imaging. World J Pediatr Congenit Heart Surg 2018;9:22-30.
27. Rychik J. The Relentless Effects of the Fontan Paradox. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2016;19:37-43.
28. Wu FM, Kogon B, Earing MG, Aboulhosn JA, Broberg CS, John AS, Harmon A, Sainani NI, Hill AL, Odze RD, Johncilla ME, Ukomadu C, Gauvreau K, Valente AM, Landzberg MJ. Liver health in adults with Fontan circulation: A multicenter cross-sectional study. J Thorac Cardiovasc Surg 2017;153:656-664.
29. Jinyoung S, Kyunghee K, June H, I-Seok K, Sung Hoon K, Ji-Hyuk Y, Tae Gook J, and Ji Hye K. Imaging Assessment of Hepatic Changes after Fontan Surgery Computed Tomography, Ultrasonography, and Transient Elastography. Int Heart J 2018;59:1008-1014.
30. Agarwala A, Cunningtonb C, Sabanayagama A, Ziera L, McCullocha CE, Harrisa IS, Fostera E, Atkinsonb D, Bryanb A, Jenkinsb P, Duab J, Parkerb MJ, Karunaratneb D, Mooreb JA, Meadowsa J, Clarkeb B, Hoschtitzkyb JA, Mahadevan VS. Cardiopulmonary exercise testing in the evaluation of liver disease in adults who have had the Fontan operation. Arch Cardiovasc Dis 2018;111:276—284.
31. Ohuchi H, Adult patients with Fontan circulation: What we know and how to manage adults with Fontan Circulation? J Cardiol 2016;68:181-189.
32. Schachter JL, Patel M, Horton SR, Devane AM, Ewing A, Abrams GA. FibroSURE and elastography poorly predict the severity of liver fibrosis in Fontan-associated liver disease. Congenit Heart Dis 2018;00:1-7.
33. Agnoletti G, Ferraro G, Bordese R, Marini D, Gala S, Bergamasco L, Ferroni F, Calvo PL, Barletti C, Cisarò F, Longo F, Pace Napoleone C. Fontan circulation causes early, severe liver damage. Should we offer patients a tailored strategy?, Int J Cardiol 2016;2019:60-65.
34. Menon S, Chennapragada M, Ugaki S, Sholler GF, Ayer J, Winlaw DS, The Lymphatic Circulation in Adaptations to the Fontan Circulation. Pediatr Cardiol 2017;38:886-892.
35. Udink Ten Cate FE, Hannes T, Germund I, Khalil M, Huntgeburth M, Apitz C, Brockmeier K, Sreeram N. Towards a proposal for a universal diagnostic definition of protein-losing enteropathy in Fontan patients: a systematic review. Heart 2016;102:1115-11159.
36. Morsheimer MM, Rychik J, Forbes L, Dodds K, Goldberg DJ, Sullivan K, Heimall JR., Risk factors and clinical significance of lymphopenia in survivors of the fontan procedure for single-ventricle congenital cardiac disease. J Allergy Clin Immunol Pract 2016;4:491-496.
37. Magdo HS, Stillwell TL, Greenhawt MJ, Stringer KA, Yu S, Fifer CG, Russell MW, Schumacher KR, Immune Abnormalities in Fontan Protein-Losing Enteropathy: A Case-Control Study. J Pediatr 2015;167:331-337.
38. Miranda C, Taqatqa A, Chapa-Rodriguez A, Holton JP, Awad SM, The Use of Fecal Calprotectin Levels in the Fontan population. Pediatr Cardiol 2018;39:591-594.
39. Allen KY, Downing TE, Glatz AC, Rogers LS, Ravishankar C, Rychik J, Fuller S, Montenegro LM, Steven JM, Spray TL, Nicolson SC, Gaynor JW, Goldberg DJ, Effect of Fontan-Associated Morbidities on Survival With Intact Fontan Circulation. Am J Cardiol 2017;119:1866-1871.
40. Unseld B, Stiller B, Borth-Bruhns T, du Bois F, Kroll J, Grohmann J, Fleck T, An Early Glenn Operation May be Associated with the Later Occurrence of Protein-Losing Enteropathy in Fontan Patients: Association of Early Glenn and Failing Fontan. Pediatr Cardiol 2017;38:1155-1161.
41. Latson L, Once More Into the Breach: A New Treatment Paradigm for Protein-Losing Enteropathy. J Am Coll Cardiol 2017;69:2938-2940.
42. John AS, Driscoll DJ, Warnes CA, Phillips SD, Cetta F. The use of oral budesonide in adolescents and adults with protein-losing enteropathy after the Fontan operation. Ann Thorac Surg 2011;92:1451–1456.
43. John AS, Johnson JA, Khan M, Driscoll DJ, Warnes CA, Cetta F. Clinical Outcomes and Improved Survival in Patients With Protein-Losing Enteropathy After the Fontan Operation. J Am Coll Cardiol 2014;64:54-62.
44. Hraška V, Decompression of Thoracic Duct: New Approach for the Treatment of Failing Fontan. Ann Thorac Surg 2013;96:709-711.
45. Itkin M, Piccoli DA, Nadolski G, Rychik J, DeWitt A, Pinto E, Rome J, Dori Y, Protein-Losing Enteropathy in Patients With Congenital Heart Disease. J Am Coll Cardiol 2017;69:2929-2937.
46. Bo Bae Jeon, M.D., Chun Soo Park, M.D., Tae-Jin Yun, Heart Transplantation in Patients with Superior Vena Cava to Pulmonary Artery Anastomosis: A Single-Institution Experience Korean. J Thorac Cardiovasc Surg 2018;51:167-171.
47. Schumacher KR, Yu S, Butts R, Castleberry C, Chen S, Edens E, Godown J, Johnson J, Kemna M, Lin K, Lowery R, Simpson K, West S, Wilmot I, Gossett JG, Fontan-associated protein-losing enteropathy and post‒heart transplant outcomes: A multicenter study. J Heart Lung Transplant. 2019;38:17-25.
48. Bacon MK, Gray SB, Schwartz SM and Cooper DS. Extracorporeal Membrane Oxygenation (ECMO) Support in Special Patient Populations—The Bidirectional Glenn and Fontan Circulations. Front Pediatr 2018;6:299.
49. Singhi AK, Vinoth B, Kuruvilla S, Sivakumar K, Plastic bronchitis. Ann Pediatr Cardiol 2015;8:246–248.
50. Schumacher KR, Singh TP, Kuebler J, Aprile K, O’Brien M, Blume ED, Risk Factors and Outcome of Fontan Associated Plastic Bronchitis: A Case-Control Study. J Am Heart Assoc 2014;3:e000865.
51. Kreutzer C, Kreutzer G, The Lymphatic System: The Achilles Heel of the Fontan-Kreutzer Circulation. World J Pediatr Congenit Heart Surg 2017;8:613-623.
52. Dori Y, Keller MS, Rychik J, Itkin M, Successful treatment of plastic bronchitis by selective lymphatic embolization in a Fontan patient. Pediatrics 2014;134:e590–e595.
53. Dori Y, Keller MS, Rome JJ, Gillespie MJ, Glatz AC, Dodds K, Goldberg DJ, Goldfarb S, RychikJ, Itkin M, Percutaneous lymphatic embolization of abnormal pulmonary lymphatic flow as treatment of plastic bronchitis in patients with congenital heart disease. Circulation 2016;133:1160–1170.
54. Collins KK, The spectrum of long-term electrophysiologic abnormalities in patients with univentricular hearts. Congenit Heart Dis 2009;4:310–317.
55. Kannankeril PJ, Anderson ME, Rottman JN, Wathen MS, Fish FA. Frequency of late recurrence of intra-atrial reentry tachycardia after radiofrequency catheter ablation in patients with congenital heart disease. Am J Cardiol 2003;92:879–881.
56. Khairy P, Fernandes SM, Mayer JE, Triedman JK, Wlash EP, Lock JE, Landznerg MJ, Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 2008;117:85–92.
57. Dahlqvist JA, Wiklund U, Karlsson M, Hanséus K, Strömvall‐Larsson E, Nygren A,·Eliasson H Rydberg A. Sinus node dysfunction in patients with Fontan circulation: could heart rate variability be a predictor for pacemaker implantation? Pediatr Cardiol 2019;40:685–693.
58. Yang H, Heidendael JF, de Groot JR, Konings TC, Veen G, van Dijk APJ, Meijboom FJ, Sieswerda JT, Post MC, Winter MM, Mulder BMJ, Bouma BJ. Oral anticoagulant therapy in adults with congenital heart disease and atrial arrhythmias: Implementation of guidelines. Int J Cardiol 2018;257;67–74.
59. Monagle P, Karl TR, Thromboembolic problems after the Fontan operation. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2002;5:36–47.
60. Monagle P, Chan AK, Goldenberg NA, Ichord RN, Journeycake JM, Nowak-Göttl U, Vesely SK, Antithrombotic therapy in neonates and children: Antithrombotic Therapy and Prevention of Thrombosis, 9th edn, American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2012;141:737–801.
61. Georgekutty J, Kazerouninia A, Wang Y, Ermis PR, Parekh DR, Lam WW. Novel oral anticoagulant use in adult Fontan patients: A single center experience. Congenit Heart Dis 2018;13:541–547.
62. Muneuchi J, Nagatomo Y, Okada S, Iida C, Shirozu H, Sugitani Y, Watanabe M, Increased Pituitary Volumes in Children after Fontan Operation: Congestion in the Other Portal Circulation. J Pediatr 2018;193:249-251.
63. Menon SC, Al-Dulaimi R, McCrindle BW, Goldberg DJ, Sachdeva R, Goldstein BH, Seery T, Uzark KC, Chelliah A, Butts R, Henderson H, Johnson T, Williams RV, Delayed puberty and abnormal anthropometry and its associations with quality of life in young Fontan survivors: A multicenter cross-sectional study. Congenit Heart Dis 2018;13:463-469.
64. Holler F, Hannes T, Germund I, Emmel M, Hoyer-Kuhn H, Khalil M, Sreeram N, Udink Ten Cate FE, Low serum 25-hydroxyvitamin D levels and secondary hyperparathyroidism in Fontan patients. Cardiol Young 2016;26:876-884.
2. Glenn WW, Circulatory by-pass of the right side of the heart - shunt between the superior vena cava and distal right pulmonary artery - report of a clinical application. N Engl J Med 1958;259:117-120.
3. Kreutzer G, Schlichter A, Laura JP, Suàrez JC, Vargas JF. Univentricular heart with low pulmonary vascular resistances: septation vs. atriopulmonary anastomosis. Arq Bras Cardiol 1981;37:301–307.
4. Björk V, Olin C, Bjarke B, Thore C. Right atrial-right ventricular anastomosis for correction of tricuspid atresia. J Thorac Cardiovasc Surg 1979;77:452–458.
5. De Leval M, Kilner P, Gewillig M, Bull C. Total cavo-pulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. Experimental studies and early clinical experience. J Thorac Cardiovasc Surg 1988;96:682-695.
6. Puga FJ, Chavareli M, Hagler DJ. Modification of the Fontan operation applicable to the patients with left atriovascular valve. Circulation 1987;76:11153–11160.
7. Marcelletti C, Corno A, Giannico S, Marino B. Inferior vena cava - pulmonary artery extracardiac conduit. A new form of right heart bypass. J Thorac Cardiovasc Surg 1990;100:228–232.
8. Gewillig M, Brown S. The Fontan circulation after 45 years: update in physiology. Heart 2016;102:1081–1086.
9. Rychik J, Fogel MA, Donofrio MT, Goldmuntz E, Cohen MS, Spray TL, Jacobs ML. Comparison of patterns of pulmonary venous blood flow in the functional single ventricle heart after operative aortopulmonary shunt versus superior cavopulmonary shunt. Am J Cardiol 1997;80:922-926.
10. Veldtman GR, Opotowsky AR, Wittekind SG, Rychik J, Penny DJ, Fogel M, Marino BS, Gewillig M. Cardiovascular adaptation to the Fontan circulation. Congenit Heart Dis 2017;12:699-710.
11. 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 2010;10:428-433.
12. Claessen G, La Gerche A, Van De Bruaene A, Claeys M, Willems R, Dymarkowski S, Bogaert J, Claus P, Budts W, Heidbuchel H, Gewillig M. Heart Rate Reserve in Fontan Patients: Chronotropic Incompetence or hemodynamic Limitation? J Am Heart Assoc 2019;8:e012008.
13. Kreutzer C, Kreutzer J, Kreutzer GO. Reflections on five decades of the Fontan Kreutzer procedure. Front Pediatr 2013;1:45.
14. Haworth SG, Reid L. Quantitative structural study of pulmonary circulation in the new-born with aortic atresia, stenosis, or coarctation. Thorax 1977;32:121-128.
15. Gewillig M, Brownb SC, Heyinga R, Eyskensa B, Ganamea J, Boshoffa DE, Budts W, Gorenflo M. Volume load paradox while preparing for the Fontan: not too much for the ventricle, not too little for the lungs. Interact Cardiovasc Thorac Surg 2010;10:262–265.
16. Khairy P, Fernandes SM, Mayer JE, Triedman JK, Walsh EP, Lock JE, Landzberg MJ. Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 2008;117:85–92.
17. Henaine R, Vergnat M, Bacha EA, Baudet B, Lambert V, Belli E, Serraf A. Effects of lack of pulsatility on pulmonary endothelial function in the Fontan circulation. J Thorac Cardiovasc Surg 2013;146:522-529.
18. Khambadkone S, Li J, De Leval MR, Cullen S, Deanfield JE, Redington AN. Basal pulmonary vascular resistance and nitric oxide responsiveness late after Fontan-type operation. Circulation 2003;107:3204-3208.
19. Hiramatsu T, Imai Y, Takanashi Y, Seo K, Terada M, Aoki M, Nakazawa M. Time Course of Endothelin-1 and Adrenomedullin After the Fontan Procedure. Ann Thorac Surg 1999;68:169–172.
20. Agnoletti G, Gala S, Ferroni F, Bordese R, Appendini L, Pace Napoleone C, Bergamasco L. Endothelin inhibitors lower pulmonary vascular resistance and improve functional capacity in patients with Fontan circulation. J Thorac Cardiovasc Surg 2017;153:1468-1475.
21. Alsaied T, Sleeper LA, Masci M, Ghelani SJ, Azcue N, Geva T, Powell AJ and Rathod RH. Maldistribution of pulmonary blood flow in patients after the Fontan operation is associated with worse exercise capacity. J Cardiovasc Magn Reson 2018;20:85.
22. Erikssen G, Aboulhosn J, Lin J, Liestøl K, Estensen ME, Gjesdal O, Skulstad H, Døhlen G, Lindberg HL. Survival in patients with univentricular hearts: the impact of right versus left ventricular morphology. Open Heart 2018;5:e000902.
23. Lastinger L, Zaidi AN. The adult with a Fontan: a panacea without a cure? Review of long-term complications. Circ J 2013;77:2672–2681.
24. Whitehead K, Gillespie MJ, Harris MA, Fogel MA, and Rome JJ. Noninvasive Quantification of Systemic To Pulmonary Collateral Flow: A Major Source of Inefficiency in Patients with Superior Cavopulmonary Connections. Circ Cardiovasc Imaging 2009;2:405–411.
25. Downing TE, Allen KY, Goldberg DJ, Rogers LS, Ravishankar C, Rychik J, Fuller S, Montenegro LM, Steven JM, Gillesple MJ, Rome JJ, Spray TL, Nicolson SC, Gaynor LW, Glatz AC. Surgical and Catheter-Based Reinterventions Are Common in Long-Term Survivors of the Fontan Operation. Circ Cardiovasc Interv 2017;10:e004924.
26. Buendìa-Fuentes F, Melero-Ferrer JL, Plaza-Lòpez D, Rueda-Soriano J, Osa-Saez A, Aguero J, Calvillo-Batllés P. Fonfria-Esparcia C, Ballesta-cunat A, Marti-Bonmati L, Martinez-Dolz L. Noninvasive Liver Assessment in Adult Patients With Fontan Circulation Using Acoustic Radiation Force Impulse Elastography and Hepatic Magnetic Resonance Imaging. World J Pediatr Congenit Heart Surg 2018;9:22-30.
27. Rychik J. The Relentless Effects of the Fontan Paradox. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2016;19:37-43.
28. Wu FM, Kogon B, Earing MG, Aboulhosn JA, Broberg CS, John AS, Harmon A, Sainani NI, Hill AL, Odze RD, Johncilla ME, Ukomadu C, Gauvreau K, Valente AM, Landzberg MJ. Liver health in adults with Fontan circulation: A multicenter cross-sectional study. J Thorac Cardiovasc Surg 2017;153:656-664.
29. Jinyoung S, Kyunghee K, June H, I-Seok K, Sung Hoon K, Ji-Hyuk Y, Tae Gook J, and Ji Hye K. Imaging Assessment of Hepatic Changes after Fontan Surgery Computed Tomography, Ultrasonography, and Transient Elastography. Int Heart J 2018;59:1008-1014.
30. Agarwala A, Cunningtonb C, Sabanayagama A, Ziera L, McCullocha CE, Harrisa IS, Fostera E, Atkinsonb D, Bryanb A, Jenkinsb P, Duab J, Parkerb MJ, Karunaratneb D, Mooreb JA, Meadowsa J, Clarkeb B, Hoschtitzkyb JA, Mahadevan VS. Cardiopulmonary exercise testing in the evaluation of liver disease in adults who have had the Fontan operation. Arch Cardiovasc Dis 2018;111:276—284.
31. Ohuchi H, Adult patients with Fontan circulation: What we know and how to manage adults with Fontan Circulation? J Cardiol 2016;68:181-189.
32. Schachter JL, Patel M, Horton SR, Devane AM, Ewing A, Abrams GA. FibroSURE and elastography poorly predict the severity of liver fibrosis in Fontan-associated liver disease. Congenit Heart Dis 2018;00:1-7.
33. Agnoletti G, Ferraro G, Bordese R, Marini D, Gala S, Bergamasco L, Ferroni F, Calvo PL, Barletti C, Cisarò F, Longo F, Pace Napoleone C. Fontan circulation causes early, severe liver damage. Should we offer patients a tailored strategy?, Int J Cardiol 2016;2019:60-65.
34. Menon S, Chennapragada M, Ugaki S, Sholler GF, Ayer J, Winlaw DS, The Lymphatic Circulation in Adaptations to the Fontan Circulation. Pediatr Cardiol 2017;38:886-892.
35. Udink Ten Cate FE, Hannes T, Germund I, Khalil M, Huntgeburth M, Apitz C, Brockmeier K, Sreeram N. Towards a proposal for a universal diagnostic definition of protein-losing enteropathy in Fontan patients: a systematic review. Heart 2016;102:1115-11159.
36. Morsheimer MM, Rychik J, Forbes L, Dodds K, Goldberg DJ, Sullivan K, Heimall JR., Risk factors and clinical significance of lymphopenia in survivors of the fontan procedure for single-ventricle congenital cardiac disease. J Allergy Clin Immunol Pract 2016;4:491-496.
37. Magdo HS, Stillwell TL, Greenhawt MJ, Stringer KA, Yu S, Fifer CG, Russell MW, Schumacher KR, Immune Abnormalities in Fontan Protein-Losing Enteropathy: A Case-Control Study. J Pediatr 2015;167:331-337.
38. Miranda C, Taqatqa A, Chapa-Rodriguez A, Holton JP, Awad SM, The Use of Fecal Calprotectin Levels in the Fontan population. Pediatr Cardiol 2018;39:591-594.
39. Allen KY, Downing TE, Glatz AC, Rogers LS, Ravishankar C, Rychik J, Fuller S, Montenegro LM, Steven JM, Spray TL, Nicolson SC, Gaynor JW, Goldberg DJ, Effect of Fontan-Associated Morbidities on Survival With Intact Fontan Circulation. Am J Cardiol 2017;119:1866-1871.
40. Unseld B, Stiller B, Borth-Bruhns T, du Bois F, Kroll J, Grohmann J, Fleck T, An Early Glenn Operation May be Associated with the Later Occurrence of Protein-Losing Enteropathy in Fontan Patients: Association of Early Glenn and Failing Fontan. Pediatr Cardiol 2017;38:1155-1161.
41. Latson L, Once More Into the Breach: A New Treatment Paradigm for Protein-Losing Enteropathy. J Am Coll Cardiol 2017;69:2938-2940.
42. John AS, Driscoll DJ, Warnes CA, Phillips SD, Cetta F. The use of oral budesonide in adolescents and adults with protein-losing enteropathy after the Fontan operation. Ann Thorac Surg 2011;92:1451–1456.
43. John AS, Johnson JA, Khan M, Driscoll DJ, Warnes CA, Cetta F. Clinical Outcomes and Improved Survival in Patients With Protein-Losing Enteropathy After the Fontan Operation. J Am Coll Cardiol 2014;64:54-62.
44. Hraška V, Decompression of Thoracic Duct: New Approach for the Treatment of Failing Fontan. Ann Thorac Surg 2013;96:709-711.
45. Itkin M, Piccoli DA, Nadolski G, Rychik J, DeWitt A, Pinto E, Rome J, Dori Y, Protein-Losing Enteropathy in Patients With Congenital Heart Disease. J Am Coll Cardiol 2017;69:2929-2937.
46. Bo Bae Jeon, M.D., Chun Soo Park, M.D., Tae-Jin Yun, Heart Transplantation in Patients with Superior Vena Cava to Pulmonary Artery Anastomosis: A Single-Institution Experience Korean. J Thorac Cardiovasc Surg 2018;51:167-171.
47. Schumacher KR, Yu S, Butts R, Castleberry C, Chen S, Edens E, Godown J, Johnson J, Kemna M, Lin K, Lowery R, Simpson K, West S, Wilmot I, Gossett JG, Fontan-associated protein-losing enteropathy and post‒heart transplant outcomes: A multicenter study. J Heart Lung Transplant. 2019;38:17-25.
48. Bacon MK, Gray SB, Schwartz SM and Cooper DS. Extracorporeal Membrane Oxygenation (ECMO) Support in Special Patient Populations—The Bidirectional Glenn and Fontan Circulations. Front Pediatr 2018;6:299.
49. Singhi AK, Vinoth B, Kuruvilla S, Sivakumar K, Plastic bronchitis. Ann Pediatr Cardiol 2015;8:246–248.
50. Schumacher KR, Singh TP, Kuebler J, Aprile K, O’Brien M, Blume ED, Risk Factors and Outcome of Fontan Associated Plastic Bronchitis: A Case-Control Study. J Am Heart Assoc 2014;3:e000865.
51. Kreutzer C, Kreutzer G, The Lymphatic System: The Achilles Heel of the Fontan-Kreutzer Circulation. World J Pediatr Congenit Heart Surg 2017;8:613-623.
52. Dori Y, Keller MS, Rychik J, Itkin M, Successful treatment of plastic bronchitis by selective lymphatic embolization in a Fontan patient. Pediatrics 2014;134:e590–e595.
53. Dori Y, Keller MS, Rome JJ, Gillespie MJ, Glatz AC, Dodds K, Goldberg DJ, Goldfarb S, RychikJ, Itkin M, Percutaneous lymphatic embolization of abnormal pulmonary lymphatic flow as treatment of plastic bronchitis in patients with congenital heart disease. Circulation 2016;133:1160–1170.
54. Collins KK, The spectrum of long-term electrophysiologic abnormalities in patients with univentricular hearts. Congenit Heart Dis 2009;4:310–317.
55. Kannankeril PJ, Anderson ME, Rottman JN, Wathen MS, Fish FA. Frequency of late recurrence of intra-atrial reentry tachycardia after radiofrequency catheter ablation in patients with congenital heart disease. Am J Cardiol 2003;92:879–881.
56. Khairy P, Fernandes SM, Mayer JE, Triedman JK, Wlash EP, Lock JE, Landznerg MJ, Long-term survival, modes of death, and predictors of mortality in patients with Fontan surgery. Circulation 2008;117:85–92.
57. Dahlqvist JA, Wiklund U, Karlsson M, Hanséus K, Strömvall‐Larsson E, Nygren A,·Eliasson H Rydberg A. Sinus node dysfunction in patients with Fontan circulation: could heart rate variability be a predictor for pacemaker implantation? Pediatr Cardiol 2019;40:685–693.
58. Yang H, Heidendael JF, de Groot JR, Konings TC, Veen G, van Dijk APJ, Meijboom FJ, Sieswerda JT, Post MC, Winter MM, Mulder BMJ, Bouma BJ. Oral anticoagulant therapy in adults with congenital heart disease and atrial arrhythmias: Implementation of guidelines. Int J Cardiol 2018;257;67–74.
59. Monagle P, Karl TR, Thromboembolic problems after the Fontan operation. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2002;5:36–47.
60. Monagle P, Chan AK, Goldenberg NA, Ichord RN, Journeycake JM, Nowak-Göttl U, Vesely SK, Antithrombotic therapy in neonates and children: Antithrombotic Therapy and Prevention of Thrombosis, 9th edn, American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2012;141:737–801.
61. Georgekutty J, Kazerouninia A, Wang Y, Ermis PR, Parekh DR, Lam WW. Novel oral anticoagulant use in adult Fontan patients: A single center experience. Congenit Heart Dis 2018;13:541–547.
62. Muneuchi J, Nagatomo Y, Okada S, Iida C, Shirozu H, Sugitani Y, Watanabe M, Increased Pituitary Volumes in Children after Fontan Operation: Congestion in the Other Portal Circulation. J Pediatr 2018;193:249-251.
63. Menon SC, Al-Dulaimi R, McCrindle BW, Goldberg DJ, Sachdeva R, Goldstein BH, Seery T, Uzark KC, Chelliah A, Butts R, Henderson H, Johnson T, Williams RV, Delayed puberty and abnormal anthropometry and its associations with quality of life in young Fontan survivors: A multicenter cross-sectional study. Congenit Heart Dis 2018;13:463-469.
64. Holler F, Hannes T, Germund I, Emmel M, Hoyer-Kuhn H, Khalil M, Sreeram N, Udink Ten Cate FE, Low serum 25-hydroxyvitamin D levels and secondary hyperparathyroidism in Fontan patients. Cardiol Young 2016;26:876-884.
Downloads
Published
03-11-2021
Issue
Section
FOCUS ON
License
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Transfer of Copyright and Permission to Reproduce Parts of Published Papers.
Authors retain the copyright for their published work. No formal permission will be required to reproduce parts (tables or illustrations) of published papers, provided the source is quoted appropriately and reproduction has no commercial intent. Reproductions with commercial intent will require written permission and payment of royalties.
How to Cite
1.
Mazza GA, Gribaudo E, Agnoletti G. The pathophysiology and complications of Fontan circulation. Acta Biomed. 2021;92(5):e2021260. doi:10.23750/abm.v92i5.10893
