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Liver fibrosis in patients with tetralogy of Fallot, an unrecognised complication?

Published online by Cambridge University Press:  15 March 2021

Maren E. H. Ravndal*
Affiliation:
Department of Paediatrics and Adolescent Medicine, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark Department of Cardiothoracic Surgery, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Lise Borgwardt
Affiliation:
Department of Clinical Physiology, Nuclear Medicine and PET, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Klaus Juul
Affiliation:
Department of Paediatrics and Adolescent Medicine, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Jon Nielsen
Affiliation:
Department of Paediatrics and Adolescent Medicine, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Lotte Borgwardt
Affiliation:
Department of Diagnostic Radiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Birthe M. Henriksen
Affiliation:
Department of Diagnostic Radiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Gro L. Willemoe
Affiliation:
Department of Pathology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Annette S. Jensen
Affiliation:
Department of Cardiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Vibeke B. Christensen
Affiliation:
Department of Paediatrics and Adolescent Medicine, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Mette S. Kjær
Affiliation:
Department of Gastroenterology and Hepatology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
*
Author for correspondence: Maren Emilie Hebeltoft Ravndal, MD, Department of Cardiothoracic Surgery, Copenhagen University Hospital, Rigshospitalet, Blegdamsvej 9, 2100, Copenhagen, Denmark. Tel: +45-35459631. E-mail: [email protected]

Abstract

Objectives:

Improved survival has led to a growing population of adults with congenital heart disease (CHD), followed by numerous reports of late complications. Liver disease is a known complication in some patients, with most studies focusing on Fontan associated liver disease. Whether liver disease also exists in other patients with CHD is not fully investigated. Elevated central venous pressure is considered pivotal in the development of liver disease in Fontan associated liver disease, and other patients with alterations in central venous pressure may also be at risk for developing liver fibrosis. We wanted to see if liver fibrosis is present in patients with tetralogy of Fallot. Many patients with tetralogy of Fallot have severe pulmonary regurgitation, which can lead to elevated central venous pressure. Patients with tetralogy of Fallot may be at risk of developing liver fibrosis.

Materials and methods:

Ten patients (24–56 years) with tetralogy of Fallot and pulmonary regurgitation were investigated for liver fibrosis. All patients were examined with magnetic resonance elastography of liver, hepatobiliary iminodiacetic acid scan, indocyanine green elimination by pulse spectrophotometry, elastography via FibroScan, abdominal ultrasound including liver elastography, and blood samples including liver markers.

Results:

Three out of ten patients had findings indicating possible liver fibrosis. Two of these had a liver biopsy performed, which revealed fibrosis stage 1 and 2, respectively. The same three patients had an estimated elevated central venous pressure in previous echocardiograms.

Conclusions:

Mild liver fibrosis was present in selected patients with tetralogy of Fallot and may be related to elevated central venous pressure.

Type
Original Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Gilboa, SM, Devine, OJ, Kucik, JE, et al. Congenital heart defects in the United States: estimating the magnitude of the affected Population in 2010. Circulation 2016; 134: 101109. doi: 10.1161/CIRCULATIONAHA.115.019307 CrossRefGoogle ScholarPubMed
Asrani, SK, Asrani, NS, Freese, DK, et al. Congenital heart disease and the liver. Hepatology 2012; 56: 11601169. doi: 10.1002/hep.25692 CrossRefGoogle ScholarPubMed
Gordon-Walker, TT, Bove, K, Veldtman, G. Fontan-associated liver disease: a review. J Cardiol 2019; 74: 223232. doi: 10.1016/j.jjcc.2019.02.016 CrossRefGoogle ScholarPubMed
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: 10011012. doi: 10.1007/s00246-012-0315-7 CrossRefGoogle Scholar
Apitz, C, Webb, GD, Redington, AN. Seminar Tetralogy of Fallot. Lancet 374: 14621471. doi: 10.1016/S0140 CrossRefGoogle Scholar
Cheung, MMH, Konstantinov, IE, Redington, AN. Late complications of repair of Tetralogy of Fallot and indications for pulmonary valve replacement. 2005. doi: 10.1053/j.semtcvs.2005.02.006 CrossRefGoogle Scholar
Chaturvedi, RR, Kilner, PJ, White, PA, Bishop, A, Szware, R, Redington, AN. Increased airway pressure and simulated branch pulmonary artery stenosis increase pulmonary regurgitation after repair of tetralogy of fallot : Real- time analysis with a conductance catheter technique. Circulation 1997; 95: 643649. doi: 10.1161/01.CIR.95.3.643 CrossRefGoogle ScholarPubMed
Rajpopat, AD, Schmidt, MR, Søndergaard, L. Time to reconsider when to re-valve for free pulmonary regurgitation in tetralogy of Fallot? EuroIntervention 2019; 14: 13441346. doi: 10.4244/EIJV14I13A242 CrossRefGoogle ScholarPubMed
Apitz, C, Latus, H, Binder, W, et al. Impact of restrictive physiology on intrinsic diastolic right ventricular function and lusitropy in children and adolescents after repair of tetralogy of Fallot. Heart 2010; 96: 18371841. doi: 10.1136/hrt.2010.203190 CrossRefGoogle ScholarPubMed
Egbe, AC, Bonnichsen, C, Reddy, YNV, Anderson, JH, Borlaug, BA. Pathophysiologic and prognostic implications of right atrial hypertension in adults with Tetralogy of Fallot. J Am Heart Assoc 2019; 8: e014148. doi: 10.1161/JAHA.119.014148 CrossRefGoogle ScholarPubMed
DiLorenzo, M, Hwang, WT, Goldmuntz, E, Ky, B, Mercer-Rosa, L. Diastolic dysfunction in tetralogy of Fallot: comparison of echocardiography with catheterization. Echocardiography 2018; 35: 16411648. doi: 10.1111/echo.14113 CrossRefGoogle ScholarPubMed
Yamamura, K, Sakamoto, I, Morihana, E, et al. Elevated non-invasive liver fibrosis markers and risk of liver carcinoma in adult patients after repair of tetralogy of Fallot. Int J Cardiol 2019; 287: 121126. doi: 10.1016/j.ijcard.2019.04.032 CrossRefGoogle ScholarPubMed
Mccabe, N, Farris, AB, Hon, H, Ford, R, Book, WM. Hepatocellular carcinoma in an adult with repaired Tetralogy of Fallot. Congenital Heart Dis 2013; 8: E139E144. doi: 10.1111/j.1747-0803.2012.00700.x Google Scholar
Augustyn, A, Peng, L, Singal, AG, Yopp, AC. Surveillance for hepatocellular carcinoma secondary to cardiogenic cirrhosis in patients with congenital heart disease. Clin Res Cardiol 2015; 104: 446449. doi: 10.1007/s00392-015-0809-4 CrossRefGoogle ScholarPubMed
Tsochatzis, EA, Bosch, J, Burroughs, AK. Liver cirrhosis. www.thelancet.com. 2014; 383. doi: 10.1016/S0140-6736(14)60121-5 CrossRefGoogle Scholar
Singh, S, Venkatesh, SK, Wang, Z, et al. Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol 2015; 13: 440451.e6. doi: 10.1016/j.cgh.2014.09.046 CrossRefGoogle ScholarPubMed
Sugimoto, M, Oka, H, Kajihama, A, et al. Non-invasive assessment of liver fibrosis by magnetic resonance elastography in patients with congenital heart disease undergoing the Fontan procedure and intracardiac repair. J Cardiol 2016; 68: 202208. doi: 10.1016/j.jjcc.2016.05.016 CrossRefGoogle ScholarPubMed
Erdogan, D, Heijnen, BHM, Bennink, RJ, et al. Preoperative assessment of liver function: a comparison of 99mTc-Mebrofenin scintigraphy with indocyanine green clearance test. Liver Int 2004; 24: 117123. doi: 10.1111/j.1478-3231.2004.00901.x CrossRefGoogle ScholarPubMed
Vos, JJ, Wietasch, JKG, Absalom, AR, Hendriks, HGD, Scheeren, TWL. Green light for liver function monitoring using indocyanine green? An overview of current clinical applications. Anaesthesia 2014; 69: 13641376. doi: 10.1111/anae.12755 CrossRefGoogle ScholarPubMed
Sakka, SG, Koeck, H, Meier-Hellmann, A. Measurement of indocyanine green plasma disappearance rate by two different dosages. Intensive Care Med 2004; 30: 506509. doi: 10.1007/s00134-003-2091-6 Google ScholarPubMed
Castéra, L, Vergniol, J, Foucher, J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005; 128: 343350. doi: 10.1053/j.gastro.2004.11.018 CrossRefGoogle ScholarPubMed
Sigrist, RMS, Liau, J, El, Kaffas A, Chammas, MC, Willmann, JK. Ultrasound elastography: Review of techniques and clinical applications. Theranostics 2017; 7: 13031329. doi: 10.7150/thno.18650 CrossRefGoogle ScholarPubMed
Bedossa, P, Poynard, T. An algorithm for the grading of activity in chronic hepatitis C. Hepatology 1996; 24: 289293. doi: 10.1002/hep.510240201 CrossRefGoogle ScholarPubMed
Zhang, J, Li, L, Jani, V, et al. Increased hepatic stiffness in young adults after biventricular repair of congenital heart disease. Ann Thorac Surg 2020. doi: 10.1016/j.athoracsur.2020.08.013 Google ScholarPubMed
DiPaola, FW, Schumacher, KR, Goldberg, CS, Friedland-Little, J, Parameswaran, A, Dillman, JR. Effect of Fontan operation on liver stiffness in children with single ventricle physiology. Eur Radiol 2017; 27: 24342442. doi: 10.1007/s00330-016-4614-x CrossRefGoogle ScholarPubMed
Millonig, G, Friedrich, S, Adolf, S, et al. Liver stiffness is directly influenced by central venous pressure. J Hepatol 2010; 52: 206210. doi: 10.1016/j.jhep.2009.11.018 CrossRefGoogle ScholarPubMed
Kutty, SS, Peng, Q, Danford, DA, et al. Increased hepatic stiffness as consequence of high hepatic afterload in the Fontan circulation: a vascular doppler and elastography study. Hepatology 2014; 59: 251260. doi: 10.1002/hep.26631 CrossRefGoogle ScholarPubMed
Bataller, R, Brenner, DA. Liver fibrosis. J Clin Invest 2005; 115: 209218. doi: 10.1172/JCI24282 CrossRefGoogle ScholarPubMed
Xanthopoulos, A, Starling, RC, Kitai, T, Triposkiadis, F. MINI-FOCUS ISSUE: CARDIAC CONSEQUENCES OF NON-CARDIAC DISEASE. Heart failure and liver disease cardiohepatic Interactions. 2019. doi: 10.1016/j.jchf.2018.10.007 CrossRefGoogle Scholar
Jalal, Z, Iriart, X, De Ledinghen, V, et al. Liver stiffness measurements for evaluation of central venous pressure in congenital heart diseases. Heart 2015; 101: 14991504. doi: 10.1136/heartjnl-2014-307385 CrossRefGoogle ScholarPubMed
Emamaullee, J, Zaidi, AN, Schiano, T, et al. Fontan-associated liver disease: screening, management, and transplant considerations. Circulation 2020; 142: 591604. doi: 10.1161/CIRCULATIONAHA.120.045597 CrossRefGoogle ScholarPubMed