End-organ consequences of the Fontan operation: Liver fibrosis, protein-losing enteropathy and plastic bronchitis

Cardiology in the Young

Volumn 23, Issue 6, 2013, Pages 830-839

  Rychik, Jack ^a   Goldberg, David ^a   Rand, Elizabeth ^a   Semeao, Edisio ^a   Russo, Pierre ^a   Dori, Yoav ^a,b   Dodds, Kathryn ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Fontan operation; liver fibrosis; plastic bronchitis; protein losing enteropathy

Indexed keywords

BOSENTAN; BUDESONIDE; SILDENAFIL; TISSUE PLASMINOGEN ACTIVATOR;

ARTICLE; BRONCHITIS; CARDIOVASCULAR MAGNETIC RESONANCE; CROUPOUS BRONCHITIS; ECHOGRAPHY; ELASTOGRAPHY; FONTAN PROCEDURE; HEART CATHETERIZATION; HEMODYNAMICS; HEPATIC VENOUS CONGESTION; HUMAN; INFLAMMATION; LIVER BIOPSY; LIVER FIBROSIS; LYMPHATIC DRAINAGE; LYMPHATIC LEAKAGE; LYMPHATIC SYSTEM DISEASE; MESENTERY BLOOD FLOW; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROTEIN LOSING GASTROENTEROPATHY; VASODILATATION; VENOUS CONGESTION; CHILD; LIVER CIRRHOSIS;

BRONCHITIS; CHILD; FONTAN PROCEDURE; HUMANS; LIVER CIRRHOSIS; PROTEIN-LOSING ENTEROPATHIES;

EID: 84892157562     PISSN: 10479511     EISSN: 14671107     Source Type: Journal    
DOI: 10.1017/S1047951113001650     Document Type: Article

References (64)

1. Rogers LS, Glatz AC, Ravishankar C, et al. 18 years of the Fontan operation at a single institution: results from 771 consecutive patients. J Am Coll Cardiol 2012; 60: 1018-1025
2. Fontan F, Baudet E. Surgical repair of tricuspid atresia. Thorax 1971; 26: 240-248
3. de Leval MR, Deanfield JE. Four decades of Fontan palliation. Nat Rev Cardiol 2010; 7: 520-527
4. Gewillig M, Brown SC, Eyskens B, et al. The Fontan circulation: who controls cardiac output? Interact Cardiovasc Thorac Surg 2010; 10: 428-433
5. de Leval MR, Dubini G, Migliavacca F, et al. Use of computational fluid dynamics in the design of surgical procedures: application to the study of competitive flows in cavo-pulmonary connections. J Thorac Cardiovasc Surg 1996; 111: 502-513
6. Penny DJ, Redington AN. Diastolic ventricular function after the Fontan operation. Am J Cardiol 1992; 69: 974-975
7. Ho PK, Lai CT, Wong SJ, Cheung YF. Three-dimensional mechanical dyssynchrony and myocardial deformation of the left ventricle in patients with tricuspid atresia after Fontan procedure. J Am Soc Echocardiogr 2012; 25: 393-400
8. Henaine R, Vergnat M, Bacha EA, et al. Effects of lack of pulsatility on pulmonary endothelial function in the Fontan circulation. J Thorac Cardiovasc Surg 2013; 146: 522-529
9. Rychik J, Fogel MA, Donofrio MT, et al. 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. Steding-Ehrenborg K, Carlsson M, Stephensen S, Arheden H. Atrial aspiration from pulmonary and caval veins is caused by ventricular contraction and secures 70% of the total stroke volume independent of resting heart rate and heart size. Clin Physiol Funct Imaging 2013; 33: 233-240
11. Gewillig M, Brown SC, Heying R, et al. 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
12. Rychik J. Forty years of the Fontan operation: a failed strategy. Seminars in thoracic and cardiovascular surgeryPediatr Cardiac Surg Ann 2010; 13: 96-100
13. Lemmer JH, Coran AG, Behrendt DM, Heidelberger KP, Stern AM. Liver fibrosis (cardiac cirrhosis) five years after modified Fontan operation for tricuspid atresia. J Thorac Cardiovasc Surg 1983; 86: 757-760
14. Schwartz MC, Sullivan L, Cohen MS, et al. Hepatic pathology may develop before the Fontan operation in children with functional single ventricle: an autopsy study. J Thorac Cardiovasc Surg 2012; 143: 904-909
15. Ghaferi AA, Hutchins GM. Progression of liver pathology in patients undergoing the Fontan procedure: chronic passive congestion, cardiac cirrhosis, hepatic adenoma, and hepatocellular carcinoma. J Thorac Cardiovasc Surg 2005; 129: 1348-1352
16. Schwartz MC, Sullivan LM, Glatz AC, et al. Portal and sinusoidal fibrosis are common on liver biopsy after Fontan surgery. Pediatr Cardiol 2013; 34: 135-142
17. Kendall TJ, Stedman B, Hacking N, et al. Hepatic fibrosis and cirrhosis in the Fontan circulation: a detailed morphological study. J Clin Pathol 2008; 61: 504-508
18. Kiesewetter CH, Sheron N, Vettukattill JJ, et al. Hepatic changes in the failing Fontan circulation. Heart 2007; 93: 579-584
19. Bryant T, Ahmad Z, Millward-Sadler H, et al. Arterialised hepatic nodules in the Fontan circulation: hepatico-cardiac interactions. Int J Cardiol 2011; 151: 268-272
20. Friedrich-Rust M, Koch C, Rentzsch A, et al. Noninvasive assessment of liver fibrosis in patients with Fontan circulation using transient elastography and biochemical fibrosis markers. J Thorac Cardiovasc Surg 2008; 135: 560-567
21. Baek JS, Bae EJ, Ko JS, et al. Late hepatic complications after Fontan operation; non-invasive markers of hepatic fibrosis and risk factors. Heart 2010; 96: 1750-1755
22. Ferraioli G, Tinelli C, Dal Bello B, et al. Accuracy of real-time shear wave elastography for assessing liver fibrosis in chronic hepatitis C: a pilot study. Hepatology 2012; 56: 2125-2133
23. Rychik J, Veldtman G, Rand E, et al. The precarious state of the liver after a Fontan operation: summary of a multidisciplinary symposium. Pediatr Cardiol 2012; 33: 1001-1012
24. Mertens L, Hagler DJ, Sauer U, Somerville J, Gewillig M. Protein-losing enteropathy after the Fontan operation: an international multicenter study. PLE study group. J Thorac Cardiovasc Surg 1998; 115: 1063-1073
25. Meadows J, Jenkins K. Protein-losing enteropathy: integrating a new disease paradigm into recommendations for prevention and treatment. Cardiol Young 2011; 21: 363-377
26. Thorne SA, Hooper J, Kemp M, Somerville J. Gastro-intestinal protein loss in late survivors of Fontan surgery and other congenital heart disease. Eur Heart J 1998; 19: 514-520
27. Rychik J. Protein-losing enteropathy after Fontan operation. Congenit Heart Dis 2007; 2: 288-300
28. Rychik J, Gui-Yang S. Relation of mesenteric vascular resistance after Fontan operation and protein-losing enteropathy. Am J Cardiol 2002; 90: 672-674
29. Uzun O, Wong JK, Bhole V, Stumper O. Resolution of proteinlosing enteropathy and normalization of mesenteric Doppler flow with sildenafil after Fontan. Ann Thorac Surg 2006; 82: e39-e40
30. Cohen MI, Rhodes LA, Wernovsky G, Gaynor JW, Spray TL, Rychik J. Atrial pacing: an alternative treatment for proteinlosing enteropathy after the Fontan operation. J Thorac Cardiovasc Surg 2001; 121: 582-583
31. Jacobs ML, Rychik J, Byrum CJ, Norwood WI Jr. Protein-losing enteropathy after Fontan operation: resolution after baffle fenestration. Ann Thorac Surg 1996; 61: 206-208
32. Rychik J, Rome JJ, Jacobs ML. Late surgical fenestration for complications after the Fontan operation. Circulation 1997; 96: 33-36
33. Bernstein D, Naftel D, Chin C, et al. Outcome of listing for cardiac transplantation for failed Fontan: a multi-institutional study. Circulation 2006; 114: 273-280
34. Ostrow AM, Freeze H, Rychik J. Protein-losing enteropathy after Fontan operation: investigations into possible pathophysiologic mechanisms. Ann Thorac Surg 2006; 82: 695-700
35. Rychik J, Piccoli DA, Barber G. Usefulness of corticosteroid therapy for protein-losing enteropathy after the Fontan procedure. Am J Cardiol 1991; 68: 819-821
36. Zellers TM, Brown K. Protein-losing enteropathy after the modified Fontan operation: oral prednisone treatment with biopsy and laboratory proved improvement. Pediatr Cardiol 1996; 17: 115-117
37. Bode L, Eklund EA, Murch S, Freeze HH. Heparan sulfate depletion amplifies TNF-alpha-induced protein leakage in an in vitro model of protein-losing enteropathy. Am J Physiol Gastrointest Liver Physiol 2005; 288: G1015-G1023.
38. Bode L, Murch S, Freeze HH. Heparan sulfate plays a central role in a dynamic in vitro model of protein-losing enteropathy. J Biol Chem 2006; 281: 7809-7815
39. Amadi B, Fagbemi AO, Kelly P, et al. Reduced production of sulfated glycosaminoglycans occurs in Zambian children with kwashiorkor but not marasmus. Am J Clin Nutr 2009; 89: 592-600
40. Thacker D, Patel A, Dodds K, Goldberg DJ, Semeao E, Rychik J. Use of oral budesonide in the management of protein-losing enteropathy after the Fontan operation. Ann Thorac Surg 2010; 89: 837-842
41. Turner Z, Lanford L, Webber S. Oral budesonide as a therapy for protein-losing enteropathy in patients having undergone Fontan palliation. Congenit Heart Dis 2012; 7: 24-30
42. Rychik J. Invited commentary. Ann Thorac Surg 2011; 92: 1456
43. 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
44. Schumacher KR, Cools M, Goldstein BH, et al. Oral budesonide treatment for protein-losing enteropathy in Fontan-palliated patients. Pediatr Cardiol 2011; 32: 966-971
45. Mertens L, Dumoulin M, Gewillig M. Effect of percutaneous fenestration of the atrial septum on protein-losing enteropathy after the Fontan operation. Br Heart J 1994; 72: 591-592
46. Kanter KR, Mahle WT, Vincent RN, Berg AM, Kogon BE, Kirshbom PM. Heart transplantation in children with a Fontan procedure. Ann Thorac Surg 2011; 91: 823-829; discussion 9-30
47. Larue M, Gossett JG, Stewart RD, Backer CL, Mavroudis C, Jacobs ML. Plastic bronchitis in patients with Fontan physiology: review of the literature and preliminary experience with Fontan conversion and cardiac transplantation. World J Pediatr Congenit Heart Surg 2012; 3: 364-372
48. Stiller B, Riedel F, Paul K, van Landeghem FK. Plastic bronchitis in children with Fontan palliation: analogue to protein-losing enteropathy? Pediatr Cardiol 2002; 23: 90-94
49. Racz J, Mane G, Ford M, et al. Immunophenotyping and protein profiling of Fontan-associated plastic bronchitis airway casts. Ann Am Thorac Soc 2013; 10: 98-107
50. Caruthers RL, Kempa M, Loo A, et al. Demographic characteristics and estimated prevalence of Fontan-associated plastic bronchitis. Pediatr Cardiol 2013; 34: 256-261
51. Wilson J, Russell J, Williams W, Benson L. Fenestration of the Fontan circuit as treatment for plastic bronchitis. Pediatr Cardiol 2005; 26: 717-719
52. Chaudhari M, Stumper O. Plastic bronchitis after Fontan operation: treatment with stent fenestration of the Fontan circuit. Heart 2004; 90: 801
53. Barber BJ, Burch GH, Tripple D, Balaji S. Resolution of plastic bronchitis with atrial pacing in a patient with Fontan physiology. Pediatr Cardiol 2004; 25: 73-76
54. Laubisch JE, Green DM, Mogayzel PJ, Reid Thompson W. Treatment of plastic bronchitis by orthotopic heart transplantation. Pediatr Cardiol 2011; 32: 1193-1195
55. ElMallah MK, Prabhakaran S, Chesrown SE. Plastic bronchitis: resolution after heart transplantation. Pediatr Pulmonol 2011; 46: 824-825
56. Haseyama K, Satomi G, Yasukochi S, Matsui H, Harada Y, Uchita S. Pulmonary vasodilation therapy with sildenafil citrate in a patient with plastic bronchitis after the Fontan procedure for hypoplastic left heart syndrome. J Thorac Cardiovasc Surg 2006; 132: 1232-1233
57. Apostolopoulou SC, Papagiannis J, Rammos S. Bosentan induces clinical, exercise and hemodynamic improvement in a pretransplant patient with plastic bronchitis after Fontan operation. J Heart Lung Transplant 2005; 24: 1174-1176
58. Costello JM, Steinhorn D, McColley S, Gerber ME, Kumar SP. Treatment of plastic bronchitis in a Fontan patient with tissue plasminogen activator: a case report and review of the literature. Pediatrics 2002; 109: e67
59. Wakeham MK, Van Bergen AH, Torero LE, Akhter J. Long-term treatment of plastic bronchitis with aerosolized tissue plasminogen activator in a Fontan patient. Pediatr Crit Care Med 2005; 6: 76-78
60. Do TB, Chu JM, Berdjis F, Anas NG. Fontan patient with plastic bronchitis treated successfully using aerosolized tissue plasminogen activator: a case report and review of the literature. Pediatr Cardiol 2009; 30: 352-355
61. Lubcke NL, Nussbaum VM, Schroth M. Use of aerosolized tissue plasminogen activator in the treatment of plastic bronchitis. Ann Pharmacother 2013; 47: e13
62. Parikh K, Witte MH, Samson R, et al. Successful treatment of plastic bronchitis with low fat diet and subsequent thoracic duct ligation in child with fontan physiology. Lymphology 2012; 45: 47-52
63. Shah SS, Drinkwater DC, Christian KG. Plastic bronchitis: is thoracic duct ligation a real surgical option? Ann Thorac Surg 2006; 81: 2281-2283
64. Ezmigna DR, Morgan WJ, Witte MH, Brown MA. Lymphoscintigraphy in plastic bronchitis, a pediatric case report. Pediatr Pulmonol 2013; 48: 515-518.