Skip to main content

Advertisement

SpringerLink
Log in

Imaging of Fontan-associated liver disease

  • Review
  • Published:
Pediatric Radiology Aims and scope Submit manuscript

Abstract

The Fontan operation has dramatically altered the natural history of functionally single ventricle congenital heart disease. Patients who have undergone the Fontan operation are living longer and, thus, noncardiac morbidity resulting from the Fontan operation is increasingly being recognized. Fontan-associated liver disease (FALD), one of the chief morbidities following the Fontan operation, is believed to be a multifactorial process that manifests as hepatic congestion and fibrosis, portal hypertension, and development of focal liver lesions, including malignant tumors. This article reviews the imaging findings of FALD in the pediatric and young adult population, reviews the literature related to the imaging of FALD and discusses possible screening algorithms for this population. The need for further research to better understand the causes of FALD, to establish if early liver stiffness measurements (or their change over time) predict long-term outcomes and complications, and to define optimal liver screening procedures is highlighted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19
Fig. 20

Similar content being viewed by others

References

  1. Prakash A, Powell AJ, Geva T (2010) Multimodality noninvasive imaging for assessment of congenital heart disease. Circ Cardiovasc Imaging 3:112–125

    PubMed  Google Scholar 

  2. Gewillig M, Brown SC (2016) The Fontan circulation after 45 years: update in physiology. Heart 102:1081–1086

    PubMed  PubMed Central  Google Scholar 

  3. Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248

    CAS  PubMed  PubMed Central  Google Scholar 

  4. de Leval MR, Kilner P, Gewillig M, Bull C (1988) Total cavopulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. Experimental studies and early clinical experience. J Thorac Cardiovasc Surg 96:682–695

    PubMed  Google Scholar 

  5. Pekkan K, Dasi LP, de Zelicourt D et al (2009) Hemodynamic performance of stage-2 univentricular reconstruction: Glenn vs. hemi-Fontan templates. Ann Biomed Eng 37:50–63

    PubMed  Google Scholar 

  6. 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

    Google Scholar 

  7. Akintoye E, Miranda WR, Veldtman GR et al (2019) National trends in Fontan operation and in-hospital outcomes in the USA. Heart 105:708–714

    PubMed  Google Scholar 

  8. Iyengar AJ, Winlaw DS, Galati JC et al (2014) The Australia and New Zealand Fontan registry: description and initial results from the first population-based Fontan registry. Intern Med J 44:148–155

    CAS  PubMed  Google Scholar 

  9. d'Udekem Y, Iyengar AJ, Cochrane AD et al (2007) The Fontan procedure: contemporary techniques have improved long-term outcomes. Circulation 116:I157–I164

    PubMed  Google Scholar 

  10. Egbe AC, Poterucha JT, Warnes CA et al (2018) Hepatocellular carcinoma after Fontan operation. Circulation 138:746–748

    PubMed  Google Scholar 

  11. Diller G-P, Kempny A, Alonso-Gonzalez R et al (2015) Survival prospects and circumstances of death in contemporary adult congenital heart disease patients under follow-up at a large tertiary Centre. Circulation 132:2118–2125

    PubMed  Google Scholar 

  12. 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

    PubMed  PubMed Central  Google Scholar 

  13. 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

    PubMed  Google Scholar 

  14. Pundi K, Pundi KN, Kamath PS et al (2016) Liver disease in patients after the Fontan operation. Am J Cardiol 117:456–460

    PubMed  Google Scholar 

  15. 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

    PubMed  Google Scholar 

  16. Koehne de Gonzalez AK, Lefkowitch JH (2017) Heart disease and the liver: pathologic evaluation. Gastroenterol Clin N Am 46:421–435

    Google Scholar 

  17. Richter S, Mucke I, Menger MD, Vollmar B (2000) Impact of intrinsic blood flow regulation in cirrhosis: maintenance of hepatic arterial buffer response. Am J Physiol Gastrointest Liver Physiol 279:G454–G462

    CAS  PubMed  Google Scholar 

  18. Kiesewetter CH, Sheron N, Vettukattill JJ et al (2007) Hepatic changes in the failing Fontan circulation. Heart 93:579–584

    PubMed  Google Scholar 

  19. Rychik J, Goldberg D, Rand E et al (2013) End-organ consequences of the Fontan operation: liver fibrosis, protein-losing enteropathy and plastic bronchitis. Cardiol Young 23:831–840

    PubMed  Google Scholar 

  20. 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

    PubMed  Google Scholar 

  21. Schwartz MC, Sullivan L, Cohen MS et al (2012) Hepatic pathology may develop before the Fontan operation in children with functional single ventricle: an autopsy study. J Thorac Cardiovasc Surg 143:904–909

    PubMed  Google Scholar 

  22. Ofei S, Gariepy C (2017) When the cause of liver disease is the heart. J Pediatr Gastroenterol Nutr 64:3–7

    PubMed  Google Scholar 

  23. Gordon-Walker TT, Bove K, Veldtman G (2019) Fontan-associated liver disease: a review. J Cardiol 74:223–232

  24. 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

    PubMed  PubMed Central  Google Scholar 

  25. Kim S-O, Lee S-Y, Jang S-I et al (2018) Hepatic stiffness using shear wave elastography and the related factors for a Fontan circulation. Pediatr Cardiol 39:57–65

    PubMed  Google Scholar 

  26. Wallihan DB, Podberesky DJ (2013) Hepatic pathology after Fontan palliation: spectrum of imaging findings. Pediatr Radiol 43:330–338

    PubMed  Google Scholar 

  27. Kim T-H, Yang HK, Jang H-J et al (2018) Abdominal imaging findings in adult patients with Fontan circulation. Insights Imaging 9:357–367

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 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

    CAS  PubMed  Google Scholar 

  29. Kendall TJ, Stedman B, Hacking N et al (2008) Hepatic fibrosis and cirrhosis in the Fontan circulation: a detailed morphological study. J Clin Pathol 61:504–508

    CAS  PubMed  Google Scholar 

  30. Sherlock S (1951) The liver in heart failure; relation of anatomical, functional, and circulatory changes. Br Heart J 13:273–293

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 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

    PubMed  Google Scholar 

  32. Yin M, Glaser KJ, Manduca A et al (2017) Distinguishing between hepatic inflammation and fibrosis with MR Elastography. Radiology 284:694–705

    PubMed  PubMed Central  Google Scholar 

  33. 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

    PubMed  Google Scholar 

  34. 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

    PubMed  Google Scholar 

  35. Elder RW, McCabe NM, Hebson C et al (2013) Features of portal hypertension are associated with major adverse events in Fontan patients: the VAST study. Int J Cardiol 168:3764–3769

    PubMed  PubMed Central  Google Scholar 

  36. Anstee QM, Dhar A, Thursz MR (2011) The role of hypercoagulability in liver fibrogenesis. Clin Res Hepatol Gastroenterol 35:526–533

    CAS  PubMed  Google Scholar 

  37. Alsaied T, Possner M, Brown N et al (2020) Lymphopenia in adults after the Fontan operation: prevalence and associations. Cardiol Young 30:641–648

    PubMed  Google Scholar 

  38. Engelhardt EM, Trout AT, Sheridan RM et al (2019) Focal liver lesions following Fontan palliation of single ventricle physiology: a radiology-pathology case series. Congenit Heart Dis 14:380–388

    PubMed  Google Scholar 

  39. Horvat N, Rocha MS, Chagas AL et al (2018) Multimodality screening of hepatic nodules in patients with congenital heart disease after Fontan procedure: role of ultrasound, ARFI elastography, CT, and MRI. AJR Am J Roentgenol 211:1212–1220

    PubMed  Google Scholar 

  40. Diaz ES, Dillman JR, Veldtman GR et al (2019) MRI measured liver stiffness does not predict focal liver lesions after the Fontan operation. Pediatr Radiol 49:99–104

    PubMed  Google Scholar 

  41. Tellez L, Rodriguez de Santiago E, Minguez B et al (2020) Prevalence, features and predictive factors of liver nodules in Fontan surgery patients: the VALDIG Fonliver prospective cohort. J Hepatol 72:702–710

    PubMed  Google Scholar 

  42. 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

    PubMed  Google Scholar 

  43. Asrani SK, Warnes CA, Kamath PS (2013) Hepatocellular carcinoma after the Fontan procedure. N Engl J Med 368:1756–1757

    CAS  PubMed  Google Scholar 

  44. Josephus Jitta D, Wagenaar LJ, Mulder BJ et al (2016) Three cases of hepatocellular carcinoma in Fontan patients: review of the literature and suggestions for hepatic screening. Int J Cardiol 206:21–26

    PubMed  Google Scholar 

  45. Wells ML, Hough DM, Fidler JL et al (2017) Benign nodules in post-Fontan livers can show imaging features considered diagnostic for hepatocellular carcinoma. Abdom Radiol (NY) 42:2623–2631

    Google Scholar 

  46. American College of Radiology (2018) CT/MR LI-RADS® v2018 core. https://www.acr.org/-/media/ACR/Files/RADS/LI-RADS/LI-RADS-2018-Core.pdf?la=en. Accessed 29 Mar 2020

  47. Di Maria MV, Brown DW, Cetta F et al (2019) Surveillance testing and preventive care after Fontan operation: a multi-institutional survey. Pediatr Cardiol 40:110–115

    PubMed  Google Scholar 

  48. Schleiger A, Salzmann M, Kramer P et al (2020) Severity of Fontan-associated liver disease correlates with Fontan hemodynamics. Pediatr Cardiol 41:736–746

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Radiology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave., Cincinnati, OH, 45229, USA

    Jonathan R. Dillman & Andrew T. Trout

  2. Department of Radiology, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    Jonathan R. Dillman & Andrew T. Trout

  3. Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    Andrew T. Trout, Tarek Alsaied & Adam M. Lubert

  4. Heart Institute, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Tarek Alsaied & Adam M. Lubert

  5. Department of Pathology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Anita Gupta

Authors
  1. Jonathan R. Dillman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew T. Trout
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tarek Alsaied
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anita Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Adam M. Lubert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan R. Dillman.

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.

CME activity

This article has been selected as the CME activity for the current month. Please visit the SPR website at www.pedrad.org on the Education page and follow the instructions to complete this CME activity.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dillman, J.R., Trout, A.T., Alsaied, T. et al. Imaging of Fontan-associated liver disease. Pediatr Radiol 50, 1528–1541 (2020). https://doi.org/10.1007/s00247-020-04776-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00247-020-04776-0

Keywords

Search

Navigation