Abstract
Background
Fontan associated liver disease (FALD) is an increasingly recognized complication of the single ventricle circulation characterized by hepatic venous congestion leading to hepatic fibrosis. Within the Fontan myocardium, fibrotic myocardial remodeling may occur and lead to ventricular dysfunction. Magnetic resonance imaging (MRI) T1 map** can characterize both myocardial and liver properties.
Objective
The aim of this study was to compare myocardial and liver T1 between single ventricle patients with and without a Fontan and biventricular controls.
Materials and methods
A retrospective study of 3 groups of patients: 16 single ventricle patients before Fontan (SVpre 2 newborns, 9 pre-Glenn, 5 pre-Fontan, 31% single right ventricle [SRV]), 16 Fontans (56% SRV) and 10 repaired d-transposition of the great arteries (TGA). Native modified Look-Locker inversion T1 times were measured in the myocardium and liver. Cardiac MRI parameters, myocardial and liver T1 values were compared in the three groups. Correlations were assessed between liver T1 and cardiac parameters.
Results
Myocardial T1 was higher in SVpre (1,056 ± 48 ms) and Fontans (1,047 ± 41 ms) compared to TGA (1,012 ± 48 ms, P < 0.05). Increased liver T1 was found in both SVpre (683 ± 82 ms) and Fontan (727 ± 49 ms) patients compared to TGA patients (587 ± 58 ms, P < 0.001). There was no difference between single left ventricle (SLV) versus SRV myocardial or liver T1. Liver T1 showed moderate correlations with myocardial T1 (r = 0.48, confidence interval [CI] 0.26–0.72) and ejection fraction (r = -0.36, CI -0.66–0.95) but not with other volumetric parameters.
Conclusion
Increased liver T1 at both pre- and post-Fontan stages suggests there are intrinsic liver abnormalities early in the course of single ventricle palliation. Increased myocardial T1 and its relationship to liver T1 suggest a combination of edema from passive venous congestion and/or myocardial fibrosis occurring in this population. Liver T1 may provide an earlier marker of liver disease warranting further study.
Similar content being viewed by others
References
Cetta F, Driscoll DJ (1997) The Fontan operation: what is it and what is its future? Cardiol Rev 5:98–104
Pudi KN, Johnson JN, Dearani JA et al (2015) 40-year follow-up after the Fontan operation: long-term outcomes of 1,052 patients. J Am Coll Cardiol 66:1700–1710
Daniels CJ, Bradley EA, Landzberg MJ et al (2017) Fontan-associated liver disease: proceedings from the American College of Cardiology Stakeholders Meeting, October 1 to 2, 2015, Washington DC. J Am Coll Cardiol 70:3173–3194
Hilscher MB, Wells ML, Venkatesh SK et al (2022) Fontan-associated liver disease. Hepatology 75:1300–1321
Camposilvan S, Milanesi O, Stellin G et al (2008) Liver and cardiac function in the long term after Fontan operation. Ann Thorac Surg 86:177–182
Ghaferi AA, Hutchins GM (2005) Progression of liver pathology in patients undergoing the Fontan procedure: chronic passive congestion, cardiac cirrhosis, hepatic adenoma, and hepatocellular carcinoma. J Thorac Cardiovasc Surg 129:1348–1352
Wallihan DB, Podberesky DJ, Marino BS et al (2014) Relationship of MR elastography determined liver stiffness with cardiac function after Fontan palliation. J Magn Reson Imaging 40:1328–1335
Rychik J, Veldtman G, Rand E et al (2012) The precarious state of the liver after a Fontan operation: summary of a multidisciplinary symposium. Pediatr Cardiol 33:1001–1012
Friedrich-Rust M, Koch C, Rentzsch A et al (2008) Noninvasive assessment of liver fibrosis in patients with Fontan circulation using transient elastography and biochemical fibrosis markers. J Thorac Cardiovasc Surg 135:560–567
Serai SD, Towbin AJ, Podberesky DJ (2012) Pediatric liver MR elastography. Dig Dis Sci 57:2713–2719
Child N, Suna G, Dabir D et al (2016) T1 map** in characterizing myocardial disease: a comprehensive review. Circ Res 119:277–299
Child N, Suna G, Dabir D et al (2018) Comparison of MOLLI, shMOLLLI, and SASHA in discrimination between health and disease and relationship with histologically derived collagen volume fraction. Eur Heart J Cardiovasc Imaging 19:768–776
Chow AM, Gao DS, Fan SJ et al (2012) Measurement of liver T(1) and T(2) relaxation times in an experimental mouse model of liver fibrosis. J Magn Reson Imaging 36:152–158
Kazour I, Serai SD, Xanthakos SA, Fleck RJ (2018) Using T1 map** in cardiovascular magnetic resonance to assess congestive hepatopathy. Abdom Radiol (NY) 43:2679–2685
Gilligan LA, Dillman JR, Tkach JA et al (2019) Magnetic resonance imaging T1 relaxation times for the liver, pancreas and spleen in healthy children at 1.5 and 3 Tesla. Pediatr Radiol 49:1018–1024
Hoffman DH, Ayoola A, Nickel D et al (2020) T1 map**, T2 map** and MR elastography of the liver for detection and staging of liver fibrosis. Abdom Radiol (NY) 45:692–700
Pagano JJ, Yim D, Lam CZ et al (2020) Normative data for myocardial native T1 and extracellular volume fraction in children. Radiol Cardiothorac Imaging 2:e190234
de Lange C, Reichert MJE, Pagano JJ et al (2019) Increased extracellular volume in the liver of pediatric Fontan patients. J Cardiovasc Magn Reson 21:39
Ramachandran P, Serai SD, Veldtman GR et al (2019) Assessment of liver T1 map** in Fontan patients and its correlation with magnetic resonance elastography-derived liver stiffness. Abdom Radiol (NY) 44:2403–2408
Shiina Y, Inai K, Ohashi R, Nagao M (2021) Potential of liver T1 map** for the detection of Fontan-associated liver disease in adults. Magn Reson Med Sci 20:295–302
Schwartz MC, Glatz AC, Daniels K et al (2015) Hepatic abnormalities are present before and early after the Fontan operation. Ann Thorac Surg 100:2298–2304
Kutty SS, Zhang M, Danford DA et al (2016) Hepatic stiffness in the bidirectional cavopulmonary circulation: The Liver Adult-Pediatric-Congenital-Heart-Disease Dysfunction Study group. J Thorac Cardiovasc Surg 151:678–684
DiPaola FW, Schumacher KR, Goldberg CS et al (2017) Effect of Fontan operation on liver stiffness in children with single ventricle physiology. Eur Radiol 27:2434–2442
Khoo NS, Smallhorn JF, Kaneko S et al (2011) Novel insights into RV adaptation and function in hypoplastic left heart syndrome between the first 2 stages of surgical palliation. JACC Cardiovasc Imaging 4:128–137
Tham EB, Smallhorn JF, Kaneko S et al (2014) Insights into the evolution of myocardial dysfunction in the functionally single right ventricle between staged palliations using speckle-tracking echocardiography. J Am Soc Echocardiogr 27:314–322
Bulut OP, Romero R, Mahle WT et al (2013) Magnetic resonance imaging identifies unsuspected liver abnormalities in patients after the Fontan procedure. J Pediatr 163:201–206
Kiesewetter CH, Sheron N, Vettukattill JJ et al (2007) Hepatic changes in the failing Fontan circulation. Heart 93:579–584
Haaf P, Garg P, Messroghli DR et al (2016) Cardiac T1 map** and extracellular volume (ECV) in clinical practice: a comprehensive review. J Cardiovasc Magn Reson 18:89
Kutty SS, Peng Q, Danford DA et al (2014) Increased hepatic stiffness as consequence of high hepatic afterload in the Fontan circulation: a vascular Doppler and elastography study. Hepatology 59:251–260
Serai SD, Wallihan DB, Venkatesh SK et al (2014) Magnetic resonance elastography of the liver in patients status-post fontan procedure: feasibility and preliminary results. Congenit Heart Dis 9:7–14
Poterucha JT, Johnson JN, Qureshi MY et al (2015) magnetic resonance elastography: a novel technique for the detection of hepatic fibrosis and hepatocellular carcinoma after the Fontan operation. Mayo Clin Proc 90:882–894
Ackerman T, Geerts A, Van Vlierberghe H et al (2018) Hepatic changes in the Fontan circulation: identification of liver dysfunction and an attempt to streamline follow-up screening. Pediatr Cardiol 39:1604–1613
Egbe A, Miranda WR, Connolly HM et al (2018) Temporal changes in liver stiffness after Fontan operation: results of serial magnetic resonance elastography. Int J Cardiol 258:299–304
Melero-Ferrer JL, Osa-Sáez A, Buendía-Fuentes F et al (2014) Fontan circulation in adult patients: acoustic radiation force impulse elastography as a useful tool for liver assessment. World J Pediatr Congenit Heart Surg 5:365–371
Mak KM, Png CYM (2020) The hepatic central vein: structure, fibrosis, and role in liver biology. Anat Rec (Hoboken) 303:1747–1767
Paris J, Henderson NC (2022) Liver zonation, revisited. Hepatology 76:1219–1230
Alsaied T, Moore RA, Lang SM et al (2020) Myocardial fibrosis, diastolic dysfunction and elevated liver stiffness in the Fontan circulation. Open Heart 7:e001434
Padalino MA, Castellani C, Toffoli S et al (2008) Pathological changes and myocardial remodelling related to the mode of shunting following surgical palliation for hypoplastic left heart syndrome. Cardiol Young 18:415–422
Ho SY, Jackson M, Kilpatrick L et al (1996) Fibrous matrix of ventricular myocardium in tricuspid atresia compared with normal heart. A quantitative analysis. Circulation 94:1642–1646
Rathod RH, Prakash A, Powell AJ, Geva T (2010) Myocardial fibrosis identified by cardiac magnetic resonance late gadolinium enhancement is associated with adverse ventricular mechanics and ventricular tachycardia late after Fontan operation. J Am Coll Cardiol 55:1721–1728
Diaz ES, Dillman JR, Veldtman GR, Trout AT (2019) MRI measured liver stiffness does not predict focal liver lesions after the Fontan operation. Pediatr Radiol 49:99–104
Tang A, Cloutier G, Szeverenyi NM, Sirlin CB (2015) Ultrasound elastography and MR elastography for assessing liver fibrosis: part 2, diagnostic performance, confounders, and future directions. AJR Am J Roentgenol 205:33–40
Kato A, Riesenkampff E, Yim D et al (2017) Pediatric Fontan patients are at risk for myocardial fibrotic remodeling and dysfunction. Int J Cardiol 240:172–177
Acknowledgements
Authors Mirza V. R. Beigh and Kiera B. E. Pajunen contributed equally to the manuscript. We wish to thank the following people for their support and assistance in this project: research coordinators Charlene Cars and Dory Sample and our cardiac MRI techs Wendy Chu, Rebecca Gray, Melissa Grzeszczak, Kelley Justice, Kam Ma and Justine Muller.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
None
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Beigh, M.V.R., Pajunen, K.B.E., Pagano, J.J. et al. T1 map** of the myocardium and liver in the single ventricle population. Pediatr Radiol 53, 1092–1099 (2023). https://doi.org/10.1007/s00247-022-05560-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00247-022-05560-y