Skip to main content
Erschienen in: Pediatric Cardiology 2/2020

18.12.2019 | Original Article

Liver Strain Using Feature Tracking of Cine Cardiac Magnetic Resonance Imaging: Assessment of Liver Dysfunction in Patients with Fontan Circulation and Tetralogy of Fallot

verfasst von: Ryoko Ohashi, Michinobu Nagao, Umiko Ishizaki, Yumi Shiina, Kei Inai, Shuji Sakai

Erschienen in: Pediatric Cardiology | Ausgabe 2/2020

Einloggen, um Zugang zu erhalten

Abstract

We propose a novel method to quantify pulsatile liver deformation using the feature tracking method of cardiac cine magnetic resonance imaging (MRI) and investigate its association with liver dysfunction in long-term postoperative patients after Fontan and intracardiac repair for the tetralogy of Fallot (TOF). Standard cine MRI which was previously performed for cardiac evaluation of 85 patients who underwent Fontan operation (mean age, 22.9 years), 43 patients with TOF (mean age, 34.6 years), and 32 healthy controls (mean age, 42.3 years) were retrospectively analyzed. Pulsatile liver deformation in the craniocaudal direction was calculated using the feature tracking method of cardiac cine imaging derived from cine-balanced turbo field-echo sequences performed on a 1.5 Tesla MR scanner, and was defined as liver strain. The liver strain was compared across the three patient groups using one-way analysis of variance. Liver dysfunction by a liver strain were compared using the Mann–Whitney U test. Liver strain for patients who underwent Fontan operation and TOF patients was significantly lower than controls (Fontan, 13.3 ± 6.5%; TOF, 15.0 ± 11.2%; controls, 23.1 ± 10.2%, p < 0.0001). In Fontan and TOF patients, MELD score was significantly greater for patients with a liver strain < 15% than those with values > 15% (5.9 ± 5.8 vs. 2.9 ± 2.9, p < 0.001). Lower liver strain values were found in adolescent and adult patients after Fontan operation and TOF, and correlates with the severity of liver injury, expressed as MELD score. Our method can evaluate hepatic function in adult congenital heart disease, together with the assessment of cardiac function.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248CrossRef Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248CrossRef
2.
Zurück zum Zitat Kreutzer G, Galindez E, Bono H, De Palma C, Laura JP (1973) An operation for the correction of tricuspid atresia. J Thorac Cardiovasc Surg 66:613–621CrossRef Kreutzer G, Galindez E, Bono H, De Palma C, Laura JP (1973) An operation for the correction of tricuspid atresia. J Thorac Cardiovasc Surg 66:613–621CrossRef
3.
Zurück zum Zitat Gates RN, Laks H, Drinkwater DC Jr, Lam L, Blitz A, Child JS et al (1997) The Fontan procedure in adults. Ann Thorac Surg 63:1085–1090CrossRef Gates RN, Laks H, Drinkwater DC Jr, Lam L, Blitz A, Child JS et al (1997) The Fontan procedure in adults. Ann Thorac Surg 63:1085–1090CrossRef
4.
Zurück zum Zitat Wolff D, van Melle JP, Ebels T, Hillege H, van Slooten YJ, Berger RM (2014) Trends in mortality (1975–2011) after one- and two-stage Fontan surgery, including bidirectional Glenn through Fontan completion. Eur J Cardiothorac Surg 45:602–609CrossRef Wolff D, van Melle JP, Ebels T, Hillege H, van Slooten YJ, Berger RM (2014) Trends in mortality (1975–2011) after one- and two-stage Fontan surgery, including bidirectional Glenn through Fontan completion. Eur J Cardiothorac Surg 45:602–609CrossRef
5.
Zurück zum Zitat Mahle WT, Spray TL, Wernovsky G, Gaynor JW, Clark BAJ (2000) Survival after reconstructive surgery for hypoplastic left heart syndrome: a 15-year experience from a single institution. Circulation 102(19 Suppl 3):III136–III141PubMed Mahle WT, Spray TL, Wernovsky G, Gaynor JW, Clark BAJ (2000) Survival after reconstructive surgery for hypoplastic left heart syndrome: a 15-year experience from a single institution. Circulation 102(19 Suppl 3):III136–III141PubMed
6.
Zurück zum Zitat Tweddell JS, Ghanayem NS, Mussatto KA, Mitchell ME, Lamers LJ, Musa NL et al (2007) Mixed venous oxygen saturation monitoring after stage 1 palliation for hypoplastic left heart syndrome. Ann Thorac Surg 84:1301–1310 discussion 1310 CrossRef Tweddell JS, Ghanayem NS, Mussatto KA, Mitchell ME, Lamers LJ, Musa NL et al (2007) Mixed venous oxygen saturation monitoring after stage 1 palliation for hypoplastic left heart syndrome. Ann Thorac Surg 84:1301–1310 discussion 1310 CrossRef
7.
Zurück zum Zitat Ohuchi H (2016) Adult patients with Fontan circulation: What we know and how to manage adults with Fontan circulation? J Cardiol 68:181–189CrossRef Ohuchi H (2016) Adult patients with Fontan circulation: What we know and how to manage adults with Fontan circulation? J Cardiol 68:181–189CrossRef
8.
Zurück zum Zitat Rychik J, Veldtman G, Rand E, Russo P, Rome JJ, Krok K et al (2012) The precarious state of the liver after a Fontan operation: summary of a multidisciplinary symposium. Pediatr Cardiol 33:1001–1012CrossRef Rychik J, Veldtman G, Rand E, Russo P, Rome JJ, Krok K et al (2012) The precarious state of the liver after a Fontan operation: summary of a multidisciplinary symposium. Pediatr Cardiol 33:1001–1012CrossRef
9.
Zurück zum Zitat Ishizaki U, Nagao M, Shiina Y, Fukushima K, Takahashi T, Shimomiya Y et al (2018) Prediction of fontan-associated liver disease using a novel cine magnetic resonance imaging “Vortex flow map” in the right atrium. Circ J 82:2143–2151CrossRef Ishizaki U, Nagao M, Shiina Y, Fukushima K, Takahashi T, Shimomiya Y et al (2018) Prediction of fontan-associated liver disease using a novel cine magnetic resonance imaging “Vortex flow map” in the right atrium. Circ J 82:2143–2151CrossRef
10.
Zurück zum Zitat Furukawa T, Akimoto K, Ohtsuki M, Sato K, Suzuki M, Takahashi K et al (2011) Non-invasive assessment of liver fibrosis in patients after the Fontan operation. Pediatr Int 53:980–984CrossRef Furukawa T, Akimoto K, Ohtsuki M, Sato K, Suzuki M, Takahashi K et al (2011) Non-invasive assessment of liver fibrosis in patients after the Fontan operation. Pediatr Int 53:980–984CrossRef
11.
Zurück zum Zitat Guha IN, Bokhandi S, Ahmad Z, Sheron N, Cope R, Marshall C et al (2011) Structural and functional uncoupling of liver performance in the Fontan circulation. Int J Cardiol 164:77–81CrossRef Guha IN, Bokhandi S, Ahmad Z, Sheron N, Cope R, Marshall C et al (2011) Structural and functional uncoupling of liver performance in the Fontan circulation. Int J Cardiol 164:77–81CrossRef
12.
Zurück zum Zitat Yamamura K, Sakamoto I, Morihana E, Hirata Y, Nagata H, Yamasaki Y et al (2019) (2019) Elevated non-invasive liver fibrosis markers and risk of liver carcinoma in afult patients after repair of tetralogy of Fallot. Int J Cardiol 287:121–126CrossRef Yamamura K, Sakamoto I, Morihana E, Hirata Y, Nagata H, Yamasaki Y et al (2019) (2019) Elevated non-invasive liver fibrosis markers and risk of liver carcinoma in afult patients after repair of tetralogy of Fallot. Int J Cardiol 287:121–126CrossRef
13.
Zurück zum Zitat Matthews JC, Pagani FD, Haft JW, Koelling TM, Naftel DC, Aaronson KD (2010) Model for end-stage liver disease score predicts left ventricular assist device operative transfusion requirements, morbidity, and mortality. Circulation 121:214–220CrossRef Matthews JC, Pagani FD, Haft JW, Koelling TM, Naftel DC, Aaronson KD (2010) Model for end-stage liver disease score predicts left ventricular assist device operative transfusion requirements, morbidity, and mortality. Circulation 121:214–220CrossRef
14.
Zurück zum Zitat Ailawadi G, Lapar DJ, Swenson BR, Siefert SA, Lau C, Kern JA et al (2009) Model for end-stage liver disease predicts mortality for tricuspid valve surgery. Ann Thorac Surg 87:1460–1467CrossRef Ailawadi G, Lapar DJ, Swenson BR, Siefert SA, Lau C, Kern JA et al (2009) Model for end-stage liver disease predicts mortality for tricuspid valve surgery. Ann Thorac Surg 87:1460–1467CrossRef
15.
Zurück zum Zitat Cholongitas E, Marelli L, Shusang V, Senzolo M, Rolles K, Patch D et al (2006) A systematic review of the performance of the model for end-stage liver disease (MELD) in the setting of liver transplantation. Liver Transpl 12:1049–1061CrossRef Cholongitas E, Marelli L, Shusang V, Senzolo M, Rolles K, Patch D et al (2006) A systematic review of the performance of the model for end-stage liver disease (MELD) in the setting of liver transplantation. Liver Transpl 12:1049–1061CrossRef
16.
Zurück zum Zitat Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, ter Borg PC (2000) A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology 31:864–871CrossRef Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, ter Borg PC (2000) A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. Hepatology 31:864–871CrossRef
17.
Zurück zum Zitat Evans WN, Acherman RJ, Ciccolo ML, Carrillo SA, Galindo A, Rothman A et al (2016) MELD-XI scores correlate with post-Fontan hepatic biopsy fibrosis scores. Pediatr Cardiol 37:1274–1277CrossRef Evans WN, Acherman RJ, Ciccolo ML, Carrillo SA, Galindo A, Rothman A et al (2016) MELD-XI scores correlate with post-Fontan hepatic biopsy fibrosis scores. Pediatr Cardiol 37:1274–1277CrossRef
18.
Zurück zum Zitat Assenza GE, Graham DA, Landzberg MJ, Valente AM, Singh MN, Bashir A et al (2013) MELDXI score and cardiac mortality or transplantation in patients after Fontan surgery. Heart 99:491–496CrossRef Assenza GE, Graham DA, Landzberg MJ, Valente AM, Singh MN, Bashir A et al (2013) MELDXI score and cardiac mortality or transplantation in patients after Fontan surgery. Heart 99:491–496CrossRef
19.
Zurück zum Zitat Friedrich-Rust M, Koch C, Rentzsch A, Sarrazin C, Schwarz P, Herrmann E et al (2008) Noninvasive assessment of liver fibrosis in patients with Fontan circulation using transient elastography and biochemical fibrosis markers. J Thorac Cardiovasc Surg 135:560–567CrossRef Friedrich-Rust M, Koch C, Rentzsch A, Sarrazin C, Schwarz P, Herrmann E et al (2008) Noninvasive assessment of liver fibrosis in patients with Fontan circulation using transient elastography and biochemical fibrosis markers. J Thorac Cardiovasc Surg 135:560–567CrossRef
20.
Zurück zum Zitat Ishizaki U, Nagao M, Shiina Y, Inai K, Mori H, Takahashi T et al (2019) Global strain and dyssynchrony of the single ventricle predict adverse cardiac events after the Fontan procedure: analysis using feature-tracking cine magnetic resonance imaging. J Cardiol 73:163–170CrossRef Ishizaki U, Nagao M, Shiina Y, Inai K, Mori H, Takahashi T et al (2019) Global strain and dyssynchrony of the single ventricle predict adverse cardiac events after the Fontan procedure: analysis using feature-tracking cine magnetic resonance imaging. J Cardiol 73:163–170CrossRef
21.
Zurück zum Zitat Shiina Y, Inai K, Takahashi T, Taniguchi K, Watanabe E, Fukushima K et al (2018) Inter- and intra-ventricular dyssynchrony in the systematic right ventricle is a surrogate marker of major cardiac events in mildly symptomatic patients. Heart Vessel 33:1086–1093CrossRef Shiina Y, Inai K, Takahashi T, Taniguchi K, Watanabe E, Fukushima K et al (2018) Inter- and intra-ventricular dyssynchrony in the systematic right ventricle is a surrogate marker of major cardiac events in mildly symptomatic patients. Heart Vessel 33:1086–1093CrossRef
22.
Zurück zum Zitat Ohuchi H, Yasuda K, Miyazaki A, Iwasa T, Sakaguchi H, Shin O et al (2014) Comparison of prognostic variables in children and adults with Fontan circulation. Int J Cardiol 173:277–283CrossRef Ohuchi H, Yasuda K, Miyazaki A, Iwasa T, Sakaguchi H, Shin O et al (2014) Comparison of prognostic variables in children and adults with Fontan circulation. Int J Cardiol 173:277–283CrossRef
23.
Zurück zum Zitat Mercer-Rosa L, Yang W, Kutty S, Rychik J, Fogel M, Goldmuntz E (2012) Quantifying pulmonary regurgitation and right ventricular function in surgically repaired tetralogy of Fallot: a comparative analysis of echocardiography and magnetic resonance imaging. Circ Cardiovasc Imaging 5:637–643CrossRef Mercer-Rosa L, Yang W, Kutty S, Rychik J, Fogel M, Goldmuntz E (2012) Quantifying pulmonary regurgitation and right ventricular function in surgically repaired tetralogy of Fallot: a comparative analysis of echocardiography and magnetic resonance imaging. Circ Cardiovasc Imaging 5:637–643CrossRef
24.
Zurück zum Zitat Yamasaki Y, Nagao M, Yamamura K, Yonezawa M, Matsuo Y, Kawanami S et al (2014) Quantitative assessment of right ventricular function and pulmonary regurgitation in surgically repaired tetralogy of Fallot using 256-slice CT: comparison with 3-Tesla MRI. Eur Radiol 24:3289–3299CrossRef Yamasaki Y, Nagao M, Yamamura K, Yonezawa M, Matsuo Y, Kawanami S et al (2014) Quantitative assessment of right ventricular function and pulmonary regurgitation in surgically repaired tetralogy of Fallot using 256-slice CT: comparison with 3-Tesla MRI. Eur Radiol 24:3289–3299CrossRef
25.
Zurück zum Zitat Guha IN, Bokhandi S, Ahmad Z, Sheron N, Cope R, Marshall C et al (2011) Structural and functional uncoupling of liver performance in the Fontan circulation. Int J Cardiol. 164:77–81CrossRef Guha IN, Bokhandi S, Ahmad Z, Sheron N, Cope R, Marshall C et al (2011) Structural and functional uncoupling of liver performance in the Fontan circulation. Int J Cardiol. 164:77–81CrossRef
26.
Zurück zum Zitat Yoo BW, Choi JY, Eun LY, Park HK, Park YH, Kim SU (2014) Congestive hepatopathy after Fontan operation and related factors assessed by transient elastography. J Thorac Cardiovasc Surg. 148:1498–1505CrossRef Yoo BW, Choi JY, Eun LY, Park HK, Park YH, Kim SU (2014) Congestive hepatopathy after Fontan operation and related factors assessed by transient elastography. J Thorac Cardiovasc Surg. 148:1498–1505CrossRef
27.
Zurück zum Zitat Yoshimitsu K, Shinagawa Y, Mitsufuji T, Mutoh E, Urakawa H, Sakamoto K et al (2017) Preliminary comparison of multi-scale and multi-model direct inversion algorithms for 3T MR elastography. Magn Reson Med Sci 16:73–77CrossRef Yoshimitsu K, Shinagawa Y, Mitsufuji T, Mutoh E, Urakawa H, Sakamoto K et al (2017) Preliminary comparison of multi-scale and multi-model direct inversion algorithms for 3T MR elastography. Magn Reson Med Sci 16:73–77CrossRef
28.
Zurück zum Zitat Kutty SS, Peng Q, Danford DA, Fletcher SE, Perry D, Talmon GA et al (2014) Liver adult-pediatric-congenital-heart-disease dysfunction study (LADS) group. Increased hepatic stiffness as consequence of high hepatic afterload in the fontan circulation: a vascular doppler and elastography study. Hepatology 59:251–260CrossRef Kutty SS, Peng Q, Danford DA, Fletcher SE, Perry D, Talmon GA et al (2014) Liver adult-pediatric-congenital-heart-disease dysfunction study (LADS) group. Increased hepatic stiffness as consequence of high hepatic afterload in the fontan circulation: a vascular doppler and elastography study. Hepatology 59:251–260CrossRef
29.
Zurück zum Zitat Chen B, Schreiber RA, Human DG, Potts JE, Guttman OR (2016) Assessment of liver stiffness in pediatric Fontan patients using transient elastography. Can J Gastroenterol Hepatol 2016:7125193CrossRef Chen B, Schreiber RA, Human DG, Potts JE, Guttman OR (2016) Assessment of liver stiffness in pediatric Fontan patients using transient elastography. Can J Gastroenterol Hepatol 2016:7125193CrossRef
30.
Zurück zum Zitat Wu FM, Opotowsky AR, Raza R, Harney S, Ukomadu C, Landzberg MJ et al (2014) Transient elastography may identify Fontan patients with unfavorable hemodynamics and advanced hepatic fibrosis. Congenit Heart Dis 9:438–447CrossRef Wu FM, Opotowsky AR, Raza R, Harney S, Ukomadu C, Landzberg MJ et al (2014) Transient elastography may identify Fontan patients with unfavorable hemodynamics and advanced hepatic fibrosis. Congenit Heart Dis 9:438–447CrossRef
Metadaten
Titel
Liver Strain Using Feature Tracking of Cine Cardiac Magnetic Resonance Imaging: Assessment of Liver Dysfunction in Patients with Fontan Circulation and Tetralogy of Fallot
verfasst von
Ryoko Ohashi
Michinobu Nagao
Umiko Ishizaki
Yumi Shiina
Kei Inai
Shuji Sakai
Publikationsdatum
18.12.2019
Verlag
Springer US
Erschienen in
Pediatric Cardiology / Ausgabe 2/2020
Print ISSN: 0172-0643
Elektronische ISSN: 1432-1971
DOI
https://doi.org/10.1007/s00246-019-02272-3

Weitere Artikel der Ausgabe 2/2020

Pediatric Cardiology 2/2020 Zur Ausgabe

Update Kardiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.