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Assessment of liver fibrosis using a 3-dimensional high-resolution late gadolinium enhancement sequence in children and adolescents with Fontan circulation

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A Publisher Correction to this article was published on 26 June 2023

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Abstract

Objectives

To assess abnormal liver enhancement on 15–20 min delayed 3D high-resolution late gadolinium enhancement (3D HR LGE) sequence in patients with Fontan circulation.

Methods

Retrospective study of pediatric Fontan patients (< 18 years old) with combined cardiac-liver MRI from January 2018 to August 2021. Abnormal hepatic enhancement was graded (0–3) for each lobe, summed for a total liver enhancement score (0–6), and compared to repaired tetralogy of Fallot (rTOF) patients. Correlations with other hepatic imaging biomarkers were performed. Temporal relationships of enhancement compared to traditional early portal venous and 5–7-min delayed phase liver imaging were analyzed.

Results

The Fontan group (n = 35, 13 ± 3.4 years old, median time from Fontan 10 (9–12) years) had 23/35 (66%) with delayed 3D HR LGE total liver enhancement score > 0 (range 0–5), with greater involvement of the right lobe (1 (0–1) vs 0 (0–1), p < 0.01). The rTOF group (n = 35, 14 ± 2.6 years old) had no abnormal enhancement. In the Fontan group, total liver enhancement was 3 (2–4) in the early portal venous phase, lower at 1 (1–2) in the 5–7-min delayed phase (p < 0.01), and lowest at 1 (0–2) in the 15–20-min delayed phase (p = 0.03). 3D HR LGE enhancement correlated inversely with portal vein flow (rs =  − 0.42, p = 0.01) and positively with left lobe stiffness (rs = 0.51, p < 0.01). The enhancement score decreased in 13/35 (37%) between the 5–7- and 15–20-min delayed phases.

Conclusions

Liver fibrosis can be assessed on 3D HR LGE sequences in patients with Fontan circulation, correlates with other imaging biomarkers of Fontan liver disease, and may add information for hepatic surveillance in this population.

Key Points

• Abnormal liver enhancement on 3D HR LGE sequences in Fontan patients likely represents liver fibrosis and is seen in up to 66% of children and adolescents with variable distribution and severity.

• The degree of 3D HR LGE liver enhancement correlates with decreased portal vein flow and increased left hepatic lobe stiffness.

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Abbreviations

3D HR LGE:

3-Dimensional high-resolution late gadolinium enhancement

3D IR FLASH:

3D inversion recovery fast low-angle shot

FALD:

Fontan-associated liver disease

MRLE:

Magnetic resonance liver elastography

rTOF:

Repaired tetralogy of Fallot

References

  1. Thrane KJ, Müller LSO, Suther KR et al (2021) Spectrum of Fontan-associated liver disease assessed by MRI and US in young adolescents. Abdom Radiol (NY) 46:3205–3216

    Article  PubMed  Google Scholar 

  2. Chavhan GB, Yoo SJ, Lam CZ, Khanna G (2021) Abdominal imaging of children and young adults with fontan circulation: pathophysiology and surveillance. AJR Am J Roentgenol 217:207–217

    Article  PubMed  Google Scholar 

  3. Dillman JR, Trout AT, Alsaied T, Gupta A, Lubert AM (2020) Imaging of Fontan-associated liver disease. Pediatr Radiol 50:1528–1541

    Article  PubMed  Google Scholar 

  4. Emamaullee J, Zaidi AN, Schiano T et al (2020) Fontan-associated liver disease: screening, management, and transplant considerations. Circulation 142:591–604

    Article  PubMed  PubMed Central  Google Scholar 

  5. Lam CZ, Gulamhusein A, Wald RM (2021) Liver cirrhosis and hepatocellular carcinoma after the fontan operation: reaching clarity in the face of uncertainty. Circulation 144:1977–1980

    Article  PubMed  Google Scholar 

  6. Wu FM, Jonas MM, Opotowsky AR et al (2015) Portal and centrilobular hepatic fibrosis in Fontan circulation and clinical outcomes. J Heart Lung Transplant 34:883–891

    Article  PubMed  Google Scholar 

  7. Goldberg DJ, Surrey LF, Glatz AC et al (2017) 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 6:e004809

    Article  PubMed  PubMed Central  Google Scholar 

  8. Surrey LF, Russo P, Rychik J et al (2016) Prevalence and characterization of fibrosis in surveillance liver biopsies of patients with Fontan circulation. Hum Pathol 57:106–115

    Article  PubMed  Google Scholar 

  9. DiPaola FW, Schumacher KR, Goldberg CS, Friedland-Little J, Parameswaran A, Dillman JR (2017) Effect of Fontan operation on liver stiffness in children with single ventricle physiology. Eur Radiol 27:2434–2442

    Article  PubMed  Google Scholar 

  10. Navallas M, Yoo SJ, Chavhan GB et al (2022) Semiquantitative characterization of dynamic magnetic resonance perfusion of the liver in pediatric Fontan patients. Pediatr Radiol 52:483–492

    Article  PubMed  Google Scholar 

  11. Wells ML, Venkatesh SK (2018) Congestive hepatopathy. Abdom Radiol (NY) 43:2037–2051

    Article  PubMed  Google Scholar 

  12. Wu FM, Ukomadu C, Odze RD, Valente AM, Mayer JE Jr, Earing MG (2011) Liver disease in the patient with fontan circulation. Congenit Heart Dis 6:190–201

    Article  PubMed  Google Scholar 

  13. Yoo SJ, Prsa M, Schantz D et al (2014) MR assessment of abdominal circulation in Fontan physiology. Int J Cardiovasc Imaging 30:1065–1072

    Article  PubMed  Google Scholar 

  14. Perucca G, de Lange C, Franchi-Abella S et al (2021) Surveillance of Fontan-associated liver disease: current standards and a proposal from the European Society of Paediatric Radiology Abdominal Task Force. Pediatr Radiol 51:2598–2606

    Article  PubMed  PubMed Central  Google Scholar 

  15. 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

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lam CZ, David D, Acosta Izquierdo L et al (2022) MRI phase contrast blood flow in fasting pediatric patients with Fontan circulation correlates with exercise capacity. Radiol Cardiothorac Imaging 4:e210303

    Article  PubMed  PubMed Central  Google Scholar 

  17. Alsaied T, Possner M, Lubert AM et al (2019) Relation of magnetic resonance elastography to Fontan failure and portal hypertension. Am J Cardiol 124:1454–1459

    Article  CAS  PubMed  Google Scholar 

  18. Lam CZ, Pagano JJ, Gill N et al (2019) Dual phase infusion with bolus tracking: technical innovation for cardiac and respiratory navigated magnetic resonance angiography using extracellular contrast. Pediatr Radiol 49:399–406

    Article  PubMed  Google Scholar 

  19. Fratz S, Chung T, Greil GF et al (2013) Guidelines and protocols for cardiovascular magnetic resonance in children and adults with congenital heart disease: SCMR expert consensus group on congenital heart disease. J Magn Reson Imaging 15:51

    Google Scholar 

  20. Landis JR, Landis KGG, Koch, (1977) The measurement of observer agreement of categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  21. Kellman P, Arai AE (2012) Cardiac imaging techniques for physicians: late enhancement. J Magn Reson Imaging 36:529–542

    Article  PubMed  PubMed Central  Google Scholar 

  22. Caro-Dominguez P, Chaturvedi R, Chavhan G et al (2019) Magnetic resonance imaging assessment of blood flow distribution in fenestrated and completed fontan circulation with special emphasis on abdominal blood flow. Korean J Radiol 20:1186–1194

    Article  PubMed  PubMed Central  Google Scholar 

  23. Rychik J, Atz AM, Celermajer DS et al (2019) Evaluation and management of the child and adult with Fontan circulation: a scientific statement from the American Heart Association. Circulation 140:e234–e284

    Article  Google Scholar 

  24. Silva-Sepulveda JA, Fonseca Y, Vodkin I et al (2019) Evaluation of Fontan liver disease: correlation of transjugular liver biopsy with magnetic resonance and hemodynamics. Congenit Heart Dis 14:600–608

    Article  PubMed  Google Scholar 

  25. Brayer SW, Zafar F, Lubert AM et al (2021) Relation of magnetic resonance elastography to fontan circulatory failure in a cohort of pediatric and adult patients. Pediatr Cardiol 42:1871–1878

    Article  PubMed  Google Scholar 

  26. Wu FM, Opotowsky AR, Raza R et al (2014) Transient elastography may identify Fontan patients with unfavorable hemodynamics and advanced hepatic fibrosis. Congenit Heart Dis 9:438–447

    Article  PubMed  Google Scholar 

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The authors state that this work has not received any funding.

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Authors and Affiliations

  1. Department of Diagnostic Imaging, Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, M5G 1X8, Canada

    Laura Acosta Izquierdo, Archana Rai, Ankavipar Saprungruang, Govind B. Chavhan, Mike Seed, Shi-Joon Yoo & Christopher Z. Lam

  2. Department of Medical Imaging, University of Toronto, Toronto, Ontario, Canada

    Laura Acosta Izquierdo, Archana Rai, Govind B. Chavhan, Mike Seed, Shi-Joon Yoo & Christopher Z. Lam

  3. Division of Cardiology, Department of Paediatrics, Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada

    Ankavipar Saprungruang, Anne I. Dipchand & Mike Seed

  4. Division of Gastroenterology, Hepatology and Nutrition, Department of Paediatrics, Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada

    Binita M. Kamath

Authors
  1. Laura Acosta Izquierdo
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  9. Christopher Z. Lam
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Correspondence to Christopher Z. Lam.

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Guarantor

The scientific guarantor of this publication is Christopher Z. Lam, MD.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise. No complex statistical methods were necessary for this paper.

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Written informed consent was waived by the Institutional Review Board.

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Methodology

•Retrospective

•Observational

•Performed at one institution

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The original online version of this article was revised: due to a typesetting mistake, the entry "Hepatic stiffness (kPa)" in Table 3 was incorrectly tagged and has now been corrected.

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Acosta Izquierdo, L., Rai, A., Saprungruang, A. et al. Assessment of liver fibrosis using a 3-dimensional high-resolution late gadolinium enhancement sequence in children and adolescents with Fontan circulation. Eur Radiol 33, 5446–5454 (2023). https://doi.org/10.1007/s00330-023-09452-z

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