Impact of the Fontan Operation on Organ Systems

Author(s): Miriam Michel*, Manuela Zlamy, Andreas Entenmann, Karin Pichler, Sabine Scholl-Bürgi, Daniela Karall, Ralf Geiger, Christina Salvador, Christian Niederwanger, Hideo Ohuchi.

Journal Name: Cardiovascular & Hematological Disorders-Drug Targets
(Formerly Current Drug Targets - Cardiovascular & Hematological Disorders)

Volume 19 , Issue 3 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

In patients having undergone the Fontan operation, besides the well discussed changes in the cardiac, pulmonary and gastrointestinal system, alterations of further organ systems including the hematologic, immunologic, endocrinological and metabolic are reported. As a medical adjunct to Fontan surgery, the systematic study of the central role of the liver as a metabolizing and synthesizing organ should allow for a better understanding of the pathomechanism underlying the typical problems in Fontan patients, and in this context, the profiling of endocrinological and metabolic patterns might offer a tool for the optimization of Fontan follow-up, targeted monitoring and specific adjunct treatment.

Keywords: Endocrinology, follow-up, fontan, gastroenterology, hepatology, hematology, immunology, metabolism.

[1]
Fontan, F.; Mounicot, F.B.; Baudet, E.; Simonneau, J.; Gordo, J.; Gouffrant, J.M. “Correction” of tricuspid atresia. 2 cases “corrected” using a new surgical technic. Ann. Chir. Thorac. Cardiovasc., 1971, 10, 39-47.
[2]
de Leval, M.R. The Fontan circulation: A challenge to William Harvey? Nat. Clin. Pract. Cardiovasc. Med., 2005, 2, 202-208.
[3]
Cheng, A.L.; Takao, C.M.; Wenby, R.B.; Meiselman, H.J.; Wood, J.C.; Detterich, J.A. Elevated low-shear blood viscosity is associated with decreased pulmonary blood flow in children with univentricular heart defects. Pediatr. Cardiol., 2016, 37(4), 789-801.
[4]
Jolley, M.; Colan, S.D.; Rhodes, J.; DiNardo, J. Fontan physiology revisited. Anesth. Analg., 2015, 121, 172-182.
[5]
Ohuchi, H. Where is the “optimal” Fontan hemodynamics. Korean Circ. J., 2017, 47, 842-857.
[6]
Gersony, W.M. Fontan operation after 3 decades: What we have learned. Circulation, 2008, 117, 13-15.
[7]
Kukreja, M.; Bryant, A.S.; Cleveland, D.C.; Dabal, R.; Hingorani, N.; Kirklin, J.K. Health-Related quality of life in adult survivors after the fontan operation. Semin. Thorac. Cardiovasc. Surg., 2015, 27, 299-306.
[8]
Uzark, K.; Zak, V.; Shrader, P.; McCrindle, B.W.; Radojewski, E.; Varni, J.W.; Daniels, K.; Handisides, J.; Hill, K.D.; Lambert, L.M.; Margossian, R.; Pemberton, V.L.; Lai, W.W.; Atz, A.M. Assessment of quality of life in young patients with single ventricle after the fontan operation. J. Pediatr., 2016, 170, 166-172.
[9]
D’Udekem, Y.; Iyengar, A.J.; Galati, J.C.; Forsdick, V.; Weintraub, R.G.; Wheaton, G.R.; Bullock, A.; Justo, R.N.; Grigg, L.E.; Sholler, G.F.; Hope, F.; Radford, D.J.; Gentles, T.L.; Celermajer, D.S.; Winlaw, D.S. Redefining expectations of long-term survival after the Fontan procedure: Twenty-five years of follow-up from the entire population of Australia and New Zealand. Circulation, 2014, 130, S32-S38.
[10]
Gewillig, M.; Goldberg, D.J. Failure of the fontan circulation. Heart Fail. Clin., 2014, 10, 105-116.
[11]
Lewis, M.; Rosenbaum, M. The miralce baby grows up: Hypoplastic left heart syndrome in the adult. Curr. Cardiol. Rep., 2017, 19(8), 74.
[http://dx.doi.org/10.1007/s11886-017-0877-3]
[12]
Marino, B.S.; Goldberg, D.J.; Dorfman, A.L.; Kind, E.; Kalkwarf, H.; Zemel, B.S.; Smith, M.; Pratt, J.; Fogel, M.A.; Shilingford, A.J.; Deal, B.J.; John, A.S.; Goldberg, C.S.; Hoffmann, T.M.; Jacobs, M.L.; Lisec, A.; Finan, S.; Kochilas, L.K.; Pawlowski, T.W.; Campbell, K.; Joiner, C.; Goldstein, S.L.; Stephens, R.; Chin, A.J. Abormalities in serum biomarkers correlate with lower cardiac index in the Fontan population. Cardiol. Young, 2017, 27(1), 59-68.
[13]
Neubauer, S. The failing heart - an engine out of fuel. N. Engl. J. Med., 2007, 356(11), 1140-1151.
[14]
Alsaied, T.; Bokma, J.P.; Engel, M.E.; Kuijpers, J.M.; Hanke, S.P.; Zuhlke, L.; Zhang, B.; Veldtman, G.R. Predicting long-term mortality after Fontan procedures: A risk score based on 6707 patients from 28 studies. Congenit. Heart Dis., 2017, 12(4), 393-398.
[15]
Talwar, S.; Singh, S.; Sreenivas, V.; Kapoor, K.S.; Gupta, S.K.; Ramakrishnan, S.; Kothari, S.S.; Saxena, A.; Juneja, R.; Choudhary, S.K.; Airan, B. Outcomes of patients undergoing primary Fontan operation beyond first decade of life. World J. Pediatr. Congenit. Heart Surg., 2017, 8(4), 487-494.
[16]
Gelatt, M.; Hamilton, R.M.; McCrindle, B.W.; Gow, R.M.; Williams, W.G.; Trusler, G.A.; Freedom, R.M. Risk factors for atrial tachyarrhythmias after the Fontan operation. J. Am. Coll. Cardiol., 1994, 24, 1735-1741.
[17]
Stephenson, E.A.; Lu, M.; Berul, C.L.; Etheridge, S.P.; Idriss, S.F.; Margossian, R.; Reed, R.H.; Prakash, A.; Sleeper, L.A.; Vetter, V.L.; Blaufox, A.D. Arrhythmias in a contemporary fontan cohort: prevalence and clinical associations in a multicenter cross-sectional study. J. Am. Coll. Cardiol., 2010, 56, 890-896.
[18]
Egbe, A.C.; Connolly, H.M.; McLeod, C.J.; Ammash, N.M.; Niaz, T.; Yogeswaran, V.; Poterucha, J.T.; Qureshi, M.Y.; Driscoll, D.J. Thrombotic and embolic complications associated with atrial arrhythmia after Fontan operation. J. Am. Coll. Cardiol., 2016, 68, 1312-1319.
[19]
Liang, F.; Senzaki, H.; Kurishima, C.; Sughimoto, K.; Inuzuka, R.; Liu, H. Hemodynamic performance of the Fontan circulation compared with a normal biventricular circulation: A computational model study. Am. J. Physiol. Heart Circ. Physiol., 2014, 307, H1056-H1072.
[20]
Anderson, P.A.; Sleeper, L.A.; Mahony, L.; Uzark, K.; Shrader, P.; Gallagher, D.; Paridon, S.M.; Williams, R.V.; Breitbart, R.E.; Colan, S.D.; Kaltman, J.R.; Margossian, R.; Pasquali, S.K.; Allen, K.; Lai, W.W.; Korsin, R.; Marino, B.S.; Mirarchi, N.; McCrindle, B.W. Contemporary outcomes after the Fontan procedure: a Pediatric Heart Network multicenter study. J. Am. Coll. Cardiol., 2008, 52, 85-98.
[21]
Michel, M.; Logoteta, J.; Entenmann, A.; Hansen, J.H.; Voges, I.; Kramer, H.H.; Petko, C. Decline of systolic and diastolic 2D Strain Rate during follow-up of HLHS patients after Fontan palliation. Pediatr. Cardiol., 2016, 37, 1250-1257.
[22]
Nakamura, Y.; Yagihara, T.; Kagisaki, K.; Hagino, I.; Kobayashi, J. Ventricular performance in long-term survivors after Fontan operation. Ann. Thorac. Surg., 2011, 91, 172-180.
[23]
Cohen, M.S.; Marino, B.S.; McElhinney, D.B.; Robbers-Visser, D.; van der Woerd, W.; Gaynor, J.W.; Spray, T.L.; Wernovsky, G. Neo-aortic root dilation and valve regurgitation up to 21 years after staged reconstruction for hypoplastic left heart syndrome. J. Am. Coll. Cardiol., 2003, 42, 533-540.
[24]
Kaulitz, R.; Ziemer, G.; Paul, T.; Peuster, M.; Bertram, H.; Hausdorf, G. Fontan-type procedures: redidual lesions and late interventions. Ann. Thorac. Surg., 2002, 74(3), 778-785.
[25]
Schumacher, K.R.; Singh, T.P.; Kuebler, J.; Aprile, K.; O’Brien, M.; Blume, E.D. Risk factors and outcome of Fontan-associated plastic bronchitis: A case-control study. J. Am. Heart Assoc., 2014, 3e000865
[26]
Ridderbos, F.J.; Wolff, D.; Timmer, A.; Van Melle, J.P.; Ebels, T.; Dickinson, M.G.; Timens, W.; Berger, R.M. Adverse pulmonary vascular remodeling in the Fontan circulation. J. Heart Lung Transplant., 2015, 34, 404-413.
[27]
Larsson, E.S.; Eriksson, B.O.; Sixt, R. Decreased lung function and exercise capacity in Fontan patients: A long-term follow-up. Scand. Cardiovasc. J., 2003, 37, 58-63.
[28]
Khiabani, R.H.; Whitehead, K.K.; Han, D.; Restrepo, M.; Tang, E.; Bethel, J.; Paridon, S.M.; Fogel, M.A.; Yoganathan, A.P. Exercise capacity in single-ventricle patients after Fontan correlates with haemodynamic energy loss in TCPC. Heart, 2015, 101, 139-143.
[29]
Ohuchi, H.; Negishi, J.; Noritake, K.; Hayama, Y.; Sakaguchi, H.; Miyazaki, A.; Kagisaki, K.; Yamada, O. Prognostic value of exercise variables in 335 patients after the fontan operation: A 23-year single-center experience of cardiopulmonary exercise testing. Congenit. Heart Dis., 2015, 10, 105-116.
[30]
Brassard, P.; Bédard, E.; Jobin, J.; Rodès-Cabau, J.; Poirier, P. Exercise capacity and impact of exercise training in patients after a Fontan procedure: A review. Can. J. Cardiol., 2006, 22(6), 489-495.
[31]
Cordina, R.; O’Meagher, S.; Gould, H.; Rae, C.; Kemp, G.; Pasco, J.A.; Celermajer, D.S.; Singh, N. Skeletal muscle abnormalities and exercise capacity in adults with a Fontan circulation. Heart, 2013, 99, 1530-1534.
[32]
Jin, S.M.; Noh, C.I.; Bae, E.J.; Choi, J.Y.; Yun, Y.S. Impaired vascular function in patients with Fontan circulation. Int. J. Cardiol., 2007, 120, 221-226.
[33]
Tomkiewicz-Pajak, L.; Dziedzic-Oleksy, H.; Pajak, J.; Olszowska, M.; Kolcz, J.; Komar, M.; Podolec, P. Arterial stiffness in adult patients after Fontan procedure. Cardiovasc. Ultrasound, 2014, 12, 15.
[34]
Ohuchi, H.; Yasuda, K.; Miyazaki, A.; Kitano, M.; Sakaguchi, H.; Yazaki, S.; Tsuda, E.; Yamada, O. Hemodynamic Characteristics before and after the onset of protein losing enteropathy in patients after the Fontan Operation. Eur. J. Cardiothorac. Surg., 2013, 43, e49-E57.
[35]
Rychik, J.; Gui-Yang, S. Relation of mesenteric vascular resistance after Fontan operation and protein-losing enteropathy. Am. J. Cardiol., 2002, 90, 672-674.
[36]
Rychik, J.; Goldberg, D.; Rand, E.; Semeao, E.; Russo, P.; Dori, Y.; Dodds, K. End-organ consequences of the Fontan operation: Liver fibrosis, protein-losing enteropathy and plastic bronchitis. Cardiol. Young, 2013, 23, 831-840.
[37]
Camposilvan, S.; Milanesi, O.; Stellin, G.; Pettenazzo, A.; Zancan, L.; D’Antiga, L. Liver and cardiac function in the long term after Fontan operation. Ann. Thorac. Surg., 2008, 86, 177-182.
[38]
Mattes, M.; Connor, J.; Kelly, S.S.; Schwartz, M.C. Lymphopenia in patients with single-ventricle heart disease after the fontan operation. Congenit. Heart Dis., 2015, 11(3), 270-275.
[39]
Ohuchi, H.; Yasuda, K.; Miyazaki, A.; Iwasa, T.; Sakaguchi, H.; Shin, O.; Mizuno, M.; Negishi, J.; Noritake, K.; Yamada, O. Comparison of prognostic variables in children and adults with Fontan circulation. Int. J. Cardiol., 2014, 173, 277-283.
[40]
Ostrow, A.M.; Freeze, H.; Rychik, J. Protein-losing enteropathy after fontan operation: Investigations into possible pathophysiologic mechanisms. Ann. Thorac. Surg., 2006, 82, 695-700.
[41]
Patel, J.K.; Loomes, K.M.; Goldberg, D.J.; Mercer-Rosa, L.; Dodds, K.; Rychik, J. Early impact of fontan operation on enteric protein loss. Ann. Thorac. Surg., 2016, 101, 1025-1030.
[42]
Kaulitz, R.; Haber, P.; Sturm, E.; Schafer, J.; Hofbeck, M. Serial evaluation of hepatic function profile after Fontan operation. Herz, 2014, 39, 98-104.
[43]
Kaulitz, R.; Luhmer, I.; Bergmann, F.; Rodeck, B.; Hausdorf, G. Sequelae after modified Fontan operation: Postoperative haemodynamic data and organ function. Heart, 1997, 78, 154-159.
[44]
Yoo, B.W.; Choi, J.Y.; Eun, L.Y.; Park, H.K.; Park, Y.H.; Kim, S.U. Congestive hepatopathy after Fontan operation and related factors assessed by transient elastography. J. Thorac. Cardiovasc. Surg., 2014, 148, 1498-1505.
[45]
van Nieuwenhuizen, R.C.; Peters, M.; Lubbers, L.J.; Trip, M.D.; Tijssen, J.G.; Mulder, B.J. Abnormalities in liver function and coagulation profile following the Fontan procedure. Heart, 1999, 82, 40-46.
[46]
Friedrich-Rust, M.; Koch, C.; Rentzsch, A.; Sarrazin, C.; Schwarz, P.; Hermann, E.; Lindinger, A.; Sarrazin, U.; Poynard, T.; Schäfers, H.J.; Zeuzem, S.; Abdul-Kaliq, H. 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.
[47]
Kutty, S.S.; Peng, Q.; Danford, D.A.; Fletcher, S.E.; Perry, D.; Talmon, G.A.; Scott, C.; Kugler, J.D.; Duncan, K.F.; Quiros-Tejeira, R.E.; Kutty, S. Increased hepatic stiffness as consequence of high hepatic afterload in the Fontan circulation: A vascular Doppler and elastography study. Hepatology, 2014, 59, 251-260.
[48]
Lindsay, I.; Johnson, J.; Everitt, M.D.; Hoffman, J.; Yetman, A.T. Impact of liver disease after the fontan operation. Am. J. Cardiol., 2015, 115, 249-252.
[49]
Mori, M.; Aguirre, A.J.; Elder, R.W.; Kashkouli, A.; Farris, A.B.; Ford, R.M.; Book, W.M. Beyond a broken heart: Circulatory dysfunction in the failing. Fontan. Pediatr. Cardiol., 2014, 35, 569-579.
[50]
Wu, F.M.; Jonas, M.M.; Opotowsky, A.R.; Harmon, A.; Raza, R.; Ukomadu, C.; Landzberg, M.J.; Singh, M.N.; Valente, A.M.; Egidy Assenza, G.; Perez-Atayde, A.R. Portal and centrilobular hepatic fibrosis in Fontan circulation and clinical outcomes. J. Heart Lung Transplant., 2015, 34(7), 883-891.
[51]
Hayashi, T.; Inuzuka, R.; Shindo, T.; Hirata, Y.; Shimizu, N.; Oka, A. Serum hyaluronic acid concentration in Fontan circulation: Correlation with hepatic function and portal vein hemodynamics. Pediatr. Cardiol., 2014, 35, 608-615.
[52]
Elder, R.W.; McCabe, N.M.; Hebson, C.; Veledar, E.; Romero, R.; Ford, R.M.; Mahle, W.T.; Kogon, B.E.; Sahu, A.; Jokhadar, M.; McConnell, M.E.; Book, W.M. Features of portal hypertension are associated with major adverse events in Fontan patients: the VAST study. Int. J. Cardiol., 2013, 168, 3764-3769.
[53]
Greenway, S.C.; Crossland, D.S.; Hudson, M.; Martin, S.R.; Myers, R.P.; Prieur, T.; Hasan, A.; Kirk, R. Fontan-associated liver disease: Implications for heart transplantation. J. Heart Lung Transplant., 2016, 35, 26-33.
[54]
Collins, N.; Piran, S.; Harrison, J.; Azevedo, E.; Oechslin, E.; Silversides, C.K. Prevalence and determinants of anemia in adults with complex congenital heart disease and ventricular dysfunction (subaortic right ventricle and single ventricle physiology). Am. J. Cardiol., 2008, 102, 625-628.
[55]
Anne, P.; Du, W.; Mattoo, T.K.; Zilberman, M.V. Nephropathy in patients after Fontan palliation. Int. J. Cardiol., 2009, 132, 244-247.
[56]
Esch, J.J.; Salvin, J.M.; Thiagarajan, R.R.; Del Nido, P.J.; Rajagopal, S.K. Acute kidney injury after Fontan completion: Risk factors and outcomes. J. Thorac. Cardiovasc. Surg., 2015, 150, 190-197.
[57]
Sharma, S.; Ruebner, R.L.; Furth, S.L.; Dodds, K.M.; Rychik, J.; Goldberg, D.J. Assessment of kidney function in survivors following Fontan palliation. Congenit. Heart Dis., 2016, 11(6), 630-636.
[58]
Opotowsky, A.R.; Baraona, F.R.; McCausland, F.R.; Loukas, B.; Landzberg, E.; Landzberg, M.J.; Sabbisetti, V.; Waikar, S.S. Estimated glomerular filtration rate and urine biomarkers in patients with single-ventricle Fontan circulation. Heart, 2017, 103(6), 434-442.
[59]
du Plessis, A.J.; Chang, A.C.; Wessel, D.L.; Lock, J.E.; Wernovsky, G.; Newburger, J.W.; Mayer, J.E. Jr. Cerebrovascular accidents following the Fontan operation. Pediatr. Neurol., 1995, 12, 230-236.
[60]
Saiki, H.; Kurishima, C.; Masutani, S.; Senzaki, H. Cerebral circulation in patients with Fontan circulation: Assessment by carotid arterial wave intensity and stiffness. Ann. Thorac. Surg., 2014, 97, 1394-1399.
[61]
Acampa, M.; Romano, D.G.; Lazzerini, P.E.; Leonini, S.; Guideri, F.; Casseri, T.; Bracco, S.; Martini, G. Increased arterial stiffness is associated with poor collaterals in acute ischemic stroke from large vessel occlusion. Curr. Neurovasc. Res., 2018, 15, 34-38.
[62]
Sarrechia, I.; Miatton, M.; De Wolf, D.; Francois, K.; Gewillig, M.; Meyns, B.; Vingerhoets, G. Neurocognitive development and behaviour in school-aged children after surgery for univentricular or biventricular congenital heart disease. Eur. J. Cardiothorac. Surg., 2016, 49(1), 167-174.
[63]
Goldberg, C.S.; Schwartz, E.M.; Brunberg, J.A.; Mosca, R.S.; Bove, E.L.; Schork, M.A.; Stetz, S.P.; Cheatham, J.P.; Kulik, T.J. Neurodevelopmental outcome of patients after the fontan operation: a comparison between children with hypoplastic left heart syndrome and other functional single ventricle lesions. J. Pediatr., 2000, 137, 646-652.
[64]
Coon, P.D.; Rychik, J.; Novello, R.T.; Ro, P.S.; Gaynor, J.W.; Spray, T.L. Thrombus formation after the Fontan operation. Ann. Thorac. Surg., 2001, 71, 1990-1994.
[65]
Tomkiewicz-Pajak, L.; Hoffman, P.; Trojnarska, O.; Lipczynska, M.; Podolec, P.; Undas, A. Abnormalities in blood coagulation, fibrinolysis, and platelet activation in adult patients after the Fontan procedure. J. Thorac. Cardiovasc. Surg., 2014, 147, 1284-1290.
[66]
Walker, H.A.; Gatzoulis, M.A. Prophylactic anticoagulation following the Fontan operation. Heart, 2005, 91, 854-856.
[67]
Balling, G. Fontan anticoagulation: A never-ending debate? J. Am. Coll. Cardiol., 2016, 68(12), 1320-1322.
[68]
Tomkiewicz-Pajak, L.; Plazak, W.; Kolcz, J.; Pajak, J.; Kopec, G.; Dluzniewska, N.; Olszowska, M.; Moryl-Bujakowska, A.; Podolec, P. Iron deficiency and hematological changes in adult patients after Fontan operation. J. Cardiol., 2014, 64, 384-389.
[69]
Magdo, H.S.; Stillwell, T.L.; Greenhawt, M.J.; Stringer, K.A.; Yu, S.; Fifer, C.G.; Russell, M.W.; Schumacher, K.R. Immune Abnormalities in fontan protein-losing enteropathy: A case-control study. J. Pediatr., 2015, 167, 331-337.
[70]
Lenz, D.; Hambsch, J.; Schneider, P.; Tarnok, A. Protein-losing enteropathy after fontan surgery: Is assessment of risk patients with immunological data possible? Cytometry B Clin. Cytom., 2003, 53, 34-39.
[71]
Lechner, E.; Gitter, R.; Mair, R.; Pinter, M.; Schreier-Lechner, E.; Vondrys, D.; Tulzer, G. Aminoterminal brain natriuretic peptide levels in children and adolescents after Fontan operation correlate with congestive heart failure. Pediatr. Cardiol., 2008, 29, 901-905.
[72]
D’Udekem, Y.; Cheung, M.M.H.; Setyapranata, S.; Iyengar, A.J.; Kelly, P.; Buckland, N.; Grigg, L.E.; Weintraub, R.G.; Vance, A.; Brizard, C.P.; Penny, D.J. How good is a good Fontan? Quality of life and exercise capacity of Fontan patients without late arrhythmia. Ann. Thorac. Surg., 2009, 88, 1961-1969.
[73]
Raedle-Hurst, T.M.; Koenigstein, K.; Gruenhage, F.; Raedle, J.; Herrmann, E.; Abdul-Khaliq, H. Growth differentiation factor 15--an early marker of abnormal function of the Fontan circuit in patients with univentricular hearts. Am. Heart J., 2010, 160, 1105-1112.
[74]
Ono, M.; Boethig, D.; Goerler, H.; Lange, M.; Westhoff-Bleck, M.; Breymann, T. Somatic development long after the Fontan operation: Factors influencing catch-up growth. J. Thorac. Cardiovasc. Surg., 2007, 134, 1199-1206.
[75]
Vogt, K.N.; Manlhiot, C.; Van Arsdell, G.; Russell, J.L.; Mital, S.; McCrindle, B.W. Somatic growth in children with single ventricle physiology impact of physiologic state. J. Am. Coll. Cardiol., 2007, 50, 1876-1883.
[76]
Holler, F.; Hannes, T.; Germund, I.; Emmel, M.; Hoyer-Kohn, H.; Khalil, M.; Sreeram, N.; Udink Ten Cate, F.E. Low serum 25-hydroxyvitamin D levels and secondary hyperparathyroidism in Fontan patients. Cardiol. Young, 2016, 26(5), 876-884.
[77]
Avitabile, C.M.; Leonard, M.B.; Zemel, B.S.; Brodsky, J.L.; Lee, D.; Dodds, K.; Hayden-Rush, C.; Whitehead, K.K.; Goldmuntz, E.; Paridon, S.M.; Rachik, S.M.; Goldberg, D.J. Lean mass deficits, vitamin D status and exercise capacity in children and young adults after Fontan palliation. Heart, 2014, 100, 1702-1707.
[78]
Ohuchi, H.; Takasugi, H.; Ohashi, H.; Yamada, O.; Watanabe, K.; Yagihara, T.; Echigo, S. Abnormalities of neurohormonal and cardiac autonomic nervous activities relate poorly to functional status in fontan patients. Circulation, 2004, 110, 2601-2608.
[79]
Ohuchi, H.; Negishi, J.; Ono, S.; Miyake, A.; Toyota, N.; Tamaki, W.; Miyazaki, A.; Yamada, O. Hyponatremia and its association with the neurohormonal activity and adverse clinical events in children and young adult patients after the Fontan operation. Congenit. Heart Dis., 2011, 6, 304-312.
[80]
Burchill, L.J.; Redington, A.N.; Silversides, C.K.; Ross, H.J.; Jimenez-Juan, L.; Mital, S.; Oechslin, E.N.; Dragulescu, A.; Slorach, C.; Mertens, L.; Wald, R.M. Renin-angiotensin-aldosterone system genotype and serum BNP in a contemporary cohort of adults late after Fontan palliation. Int. J. Cardiol., 2015, 197, 209-215.
[81]
Ohuchi, H.; Negishi, J.; Miyake, A.; Sakaguchi, H.; Miyazaki, A.; Yamada, O. Long-term prognostic value of cardiac autonomic nervous activity in postoperative patients with congenital heart disease. Int. J. Cardiol., 2011, 151, 296-302.
[82]
Acampa, M.; Lazzerini, P.E.; Martini, G. Atrial cardiopathy and sympatho-vagal imbalance in cryptogenic stroke: Pathogenic mechanisms and effects on electrocardiographic markers. Front. Neurol., 2018, 9, 469.
[83]
Ohuchi, H.; Negishi, J.; Hayama, Y.; Sasaki, O.; Taniguchi, Y.; Noritake, K.; Miyazaki, A.; Yamada, O. Hyperuricemia reflects global Fontan pathophysiology and associates with morbidity and mortality in patients after the Fontan operation. Int. J. Cardiol., 2015, 184, 623-630.
[84]
Ohuchi, H.; Miyamoto, Y.; Yamamoto, M.; Ishihara, H.; Takata, H.; Miyazaki, A.; Yamada, O.; Yagihara, T. High prevalence of abnormal glucose metabolism in young adult patients with complex congenital heart disease. Am. Heart J., 2009, 158, 30-39.
[85]
Ohuchi, H.; Yasuda, K.; Ono, S.; Hayama, Y.; Megishi, J.; Noritake, K.; Mizuno, M.; Iwasa, T.; Miyazaki, A.; Yamada, O. Low fasting plasma glucose level predicts morbidity and mortality in symptomatic adults with congenital heart disease. Int. J. Cardiol., 2014, 174, 306-312.
[86]
Whiteside, W.; Tan, M.; Ostlund, R.E. Jr., Yu, S.; Ma, L.; Rocchini, A. Altered cholesterol metabolism and hypocholesterolemia in patients with single ventricle following fontan palliation. J. Pediatr., 2016, 171, 73-77.
[87]
Whiteside, W.; Tan, M.; Yu, S.; Rocchini, A. Low total, low-density lipoprotein, high-density lipoprotein, and non-high-density lipoprotein cholesterol levels in patients with complex congenital heart disease after Fontan palliation. J. Pediatr., 2013, 162, 1199-1204.
[88]
Zyblewski, S.C.; Argraves, W.S.; Graham, E.M.; Slate, E.H.; Atz, A.M.; Bradley, S.M.; McQuinn, T.C.; Wilkerson, B.A.; Wing, S.B.; Argraves, K.M. Reduction in postoperative high-density lipoprotein cholesterol levels in children undergoing the Fontan operation. Pediatr. Cardiol., 2012, 33, 1154-1159.
[89]
Yancy, C.W.; Jessup, M.; Bozkurt, B.; Butler, J.; Casey, D.E. Jr, Colvin, M.M.; Drazner, M.H.; Filippatos, G.S.; Fonarow, G.C.; Givertz, M.M.; Hollenberg, S.M.; Lindenfeld, J.; Masoudi, F.A.; McBride, P.E.; Peterson, P.N.; Stevenson, L.W.; Westlake, C. 2017 ACC/AHA/HFSA Focused Update of the 2013 ACCF/AHA Guideline for the Management of Heart Failure: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Failure Society of America. Circulation, 2017, 136, e137-e161.
[90]
Ventura-Clapier, R.; Garnier, A.; Veksler, V. Energy metabolism in heart failure. J. Physiol., 2004, 555, 1-13.
[91]
Chung, S.T.; Hong, B.; Patterson, L.; Petit, C.J.; Ham, J.N. High overweight and obesity in fontan patients: A 20-year history. Pediatr. Cardiol., 2016, 37, 192-200.
[92]
Shibayama, J.; Yuzyuk, T.N.; Cox, J.; Makaju, A.; Miller, M.; Lichter, J.; Li, H.; Leavy, J.D.; Franklin, S.; Zaitsev, A.V. Metabolic remodeling in moderate synchronous versus dyssynchronous pacing-induced heart failure: Integrated metabolomics and proteomics study. PLoS One, 2015, 10e0118974
[93]
Gehmlich, K.; Dodd, M.S.; Allwood, J.W.; Kelly, M.; Bellahcene, M.; Lad, H.V.; Stockenhuber, A.; Hooper, C.; Ashrafian, H.; Redwood, C.S.; Carrier, L.; Dunn, W.B. Changes in the cardiac metabolome caused by perhexiline treatment in a mouse model of hypertrophic cardiomyopathy. Mol. Biosyst., 2015, 11, 564-573.
[94]
Lai, L.; Leone, T.C.; Keller, M.P.; Martin, O.J.; Broman, A.T.; Nigro, J.; Kapoor, K.; Koves, T.R.; Stevens, R.; Ilkayeva, O.R.; Vega, R.B. ATtie, A.D.; Muoio, D.M.; Kelly, D.P. Energy metabolic reprogramming in the hypertrophied and early stage failing heart: A multisystems approach. Circ Heart Fail, 2014, 7, 1022-1031.
[95]
Hill, B.G.; Schulze, P.C. Insights into metabolic remodeling of the hypertrophic and failing myocardium. Circ Heart Fail, 2014, 7, 874-876.
[96]
Aubert, G.; Martin, O.J.; Horton, J.L.; Lai, L.; Vega, R.B.; Leone, T.C.; Koves, T.; Gardell, S.J.; Krüger, M.; Hoppel, C.L.; Lewandowski, E.D.; Crawford, P.A.; Muoio, D.M.; Kelly, D.P. The failing heart relies on ketone bodies as a fuel. Circulation, 2006, 133, 698-705.
[97]
Bedi, K.C. Jr., Snyder, N.W.; Brandimarto, J.; Aziz, M.; Mesaros, C.; Worth, A.J.; Wang, L.L.; Javaheri, A.; Blair, I.A.; Margulies, K.B.; Rame, J.E. Evidence for intramyocardial disruption of lipid metabolism and increased myocardial ketone utilization in advanced human heart failure. Circulation, 2016, 133, 706-716.
[98]
Zordoky, B.N.; Sung, M.M.; Ezekowitz, J.; Mandal, R.; Han, B.; Bjorndahl, T.C.; Bouatra, S.; Anderson, T.; Oudit, G.Y.; Wishart, D.S.; Dyck, J.R. Metabolomic fingerprint of heart failure with preserved ejection fraction. PLoS One, 2015, 10(5)e0124844
[99]
Goldberg, D.J.; Surrey, L.F.; Glatz, A.C.; Dodds, K.; O’Byrne, M.L.; Lin, H.C.; Fogel, M.; Rome, J.J.; Rand, E.B.; Russo, P.; Rychik, J. Hepatic fibrosis is universal following Fontan operation, and severity is associated with time from surgery: A liver biopsy and hemodynamic study. J. Am. Heart Assoc., 2017, 6e004809
[100]
Mizuno, M.; Ohuchi, H.; Matsuyama, T.A.; Miyazaki, A.; Ishibashi-Ueda, H.; Yamada, O. Diverse multi-organ histopathologic changes in a failed Fontan patient. Pediatr. Int. , 2016, 58, 1061-1065.
[101]
Furukawa, T.; Akimoto, K.; Ohtsuki, M.; Sato, K.; Suzuki, M.; Takahashi, K.; Kishiro, M.; Shimizu, T.; Kawasaki, S. Non-invasive assessment of liver fibrosis in patients after the Fontan operation. Pediatr. Int., 2011, 53, 980-984.
[102]
Kothari, S.S. Non-cardiac issues in patients with heterotaxy syndromes. Ann. Pediatr. Cardiol., 2014, 7, 187-192.
[103]
Goldberg, D.J.; Surrey, L.F.; Glatz, A.C.; Dodds, K.; O’Byrne, M.L.; Lin, H.C.; Fogel, M.; Rome, J.J.; Rand, E.B.; Russo, P.; Rychik, J. Hepatic fibrosis is universal following Fontan operation, and severity is associated with time from surgery: A liver biopsy and hemodynamic study. J. Am. Heart Assoc., 2017, 6 pii: e004809
[http://dx.doi.org/10.1161/JAHA.116.004809]
[104]
Daley, M.; d’Udekem, Y. In patients undergoing Fontan completion, does a younger age at operation result in better long-term exercise capacity and prognosis? Interact. Cardiovasc. Thorac. Surg., 2018.
[http://dx.doi.org/10.1093/icvts/ivy219]
[105]
Garcia Ropero, A.; Baskar, S.; Roos Hesselink, J.W.; Girnius, A.; Zentner, D.; Swan, L.; Ladouceur, M.; Brown, N.; Veldtman, G.R. Pregnancy in women with a Fontan circulation: A systematic review of the literature. Circ. Cardiovasc. Qual. Outcomes, 2018, 11e004575
[http://dx.doi.org/10.1161/CIRCOUTCOMES.117.004575]
[106]
Rajpal, S.; Alshawabkeh, L.; Opotowsky, A.R. Current role of blood and urine biomarkers in the clinical care of adults with congenital heart disease. Curr. Cardiol. Rep., 2017, 19(6), 50.
[107]
Fridman, M.D.; Mital, S. Perspective on precision medicine in paediatric heart failure. Clin. Sci. (Lond.), 2017, 131(6), 439-448.
[108]
Hansson, L.; Ohlund, I.; Lind, T.; Stecksen-Blicks, C.; Rydberg, A. Dietary intake in infants with complex congenital heart disease: A case-control study on macro- and micronutrient intake, meal frequency and growth. J. Hum. Nutr. Diet., 2014, 29(1), 67-74.
[109]
Zukunft, S.; Sorgenfrei, M.; Prehn, C.; Möller, G.; Adamski, J. Targeted Metabolomics of dried blood spot extracts. Chromatographia, 2013, 76, 1295-1305.
[110]
Peng, G.; Hakim, M.; Broza, Y.Y.; Billan, S.; Abdah-Bortnyak, R.; Kuten, A.; Tisch, U.; Haick, H. Detection of lung, breast, colorectal, and prostate cancers from exhaled breath using a single array of nanosensors. Br. J. Cancer, 2010, 103(4), 542-551.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 3
Year: 2019
Page: [205 - 214]
Pages: 10
DOI: 10.2174/1871529X19666190211165124
Price: $58

Article Metrics

PDF: 29
HTML: 4

Special-new-year-discount