Skip to main content
Log in

Semiquantitative characterization of dynamic magnetic resonance perfusion of the liver in pediatric Fontan patients

  • Original Article
  • Published:
Pediatric Radiology Aims and scope Submit manuscript

Abstract

Background

Dynamic contrast-enhanced magnetic resonance imaging (MRI) of the liver in pediatric Fontan patients often shows peripheral reticular areas of hypoenhancement, which has not been studied in detail.

Objective

To semiquantitatively score the hepatic MR perfusion abnormality seen in pediatric Fontan patients, and to correlate the perfusion abnormality with functional clinical and hemodynamic parameters.

Materials and methods

All children (< 18 years old) after Fontan palliation with combined clinical cardiac and liver MRI performed between May 2017 and April 2019 were considered for inclusion. A semiquantitative perfusion score was used to assess the severity of the hepatic reticular pattern seen on dynamic contrast-enhanced liver imaging. The liver was divided into four sections: right posterior, right anterior, left medial and left lateral. Each liver section was assigned a score from 0 to 4 depending on the amount of abnormal reticular hypoenhancement. Scoring was assigned for each section of the liver across eight successive dynamic contrast-enhanced modified spoiled gradient echo runs. Scores were correlated with clinical and hemodynamic parameters.

Results

All Fontan children showed hepatic reticular hypoenhancement by MRI, most severe in the early portal venous phase with a median maximum total perfusion abnormality score of 12 (range: 9–14). All perfusion abnormalities progressively resolved during the hepatic venous phase. Perfusion abnormality scores were greatest in the right compared to left hepatic lobes (7 range: [6–8] vs. 5 [range: 3–6], P < 0.01). The maximum left hepatic lobe perfusion abnormality scores were greatest in children with versus without imaging signs of portal hypertension (8 [range: 7–8] vs. 4 [range: 3–5], P < 0.01). High unconjugated bilirubin and low platelets correlated with greater perfusion abnormality (R = 0.450, P = 0.024, and R =  − 0.458, P < 0.01, respectively). Age at MRI, time from Fontan, focal liver lesions and cardiac MRI hemodynamic parameters did not show significant correlations with the severity of the liver perfusion abnormality.

Conclusion

All Fontan children have hepatic reticular hypoenhancement abnormalities seen with MRI that are most severe in the right hepatic lobe and universally show gradual resolution through the hepatic venous phase. Perfusion abnormality in the left hepatic lobe is worse in children with portal hypertension.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Cowgill LD (1991) The Fontan procedure: a historical review. Ann Thorac Surg 51:1026–1030

    Article  CAS  Google Scholar 

  2. Gewillig M, Brown SC, van de Bruaene A, Rychik J (2020) Providing a framework of principles for conceptualising the Fontan circulation. Acta Paediatr 109:651–658

    Article  Google Scholar 

  3. de Lange C (2020) Imaging of complications following Fontan circulation in children — diagnosis and surveillance. Pediatr Radiol 50:1333–1348

    Article  Google Scholar 

  4. Pundi 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

    Article  Google Scholar 

  5. 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

    Article  Google Scholar 

  6. Khanna G, Bhalla S, Krishnamurthy R, Canter C (2012) Extracardiac complications of the Fontan circuit. Pediatr Radiol 42:233–241

    Article  Google Scholar 

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

    Article  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. Bavil EA, Yang HK, Doyle MG et al (2020) Cardiovascular and abdominal flow alterations in adults with morphologic evidence of liver disease post Fontan palliation. Int J Cardiol 317:63–69

    Article  Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. Agnoletti G, Ferraro G, Bordese R et al (2016) Fontan circulation causes early, severe liver damage. Should we offer patients a tailored strategy? Int J Cardiol 209:60–65

    Article  Google Scholar 

  12. 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Rathgeber SL, Guttman OR, Lee AF et al (2020) Fontan-associated liver disease: spectrum of disease in children and adolescents. J Am Heart Assoc 9:e012529

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  16. 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  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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. https://doi.org/10.1161/CIR.0000000000000696

    Article  PubMed  Google Scholar 

  19. Dillman JR, Trout AT, Alsaied T et al (2020) Imaging of Fontan-associated liver disease. Pediatr Radiol 50:1528–1541

    Article  Google Scholar 

  20. Chavhan GB, Yoo S-J, 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  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. Megremis SD, Vlachonikolis IG, Tsilimigaki AM (2004) Spleen length in childhood with US: normal values based on age, sex, and somatometric parameters. Radiology 231:129–134

    Article  Google Scholar 

  23. Konuş OL, Ozdemir A, Akkaya A et al (1998) Normal liver, spleen, and kidney dimensions in neonates, infants, and children: evaluation with sonography. AJR Am J Roentgenol 171:1693–1698

    Article  Google Scholar 

  24. Harbin WP, Robert NJ, Ferrucci JT Jr (1980) Diagnosis of cirrhosis based on regional changes in hepatic morphology: a radiological and pathological analysis. Radiology 135:273–283

    Article  CAS  Google Scholar 

  25. Dillman JR, Serai SD, Trout AT et al (2019) Diagnostic performance of quantitative magnetic resonance imaging biomarkers for predicting portal hypertension in children and young adults with autoimmune liver disease. Pediatr Radiol 49:332–341

    Article  Google Scholar 

  26. Bloom S, Kemp W, Lubel J (2015) Portal hypertension: pathophysiology, diagnosis and management. Intern Med J 45:16–26

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Wu FM, Kogon B, Earing MG et al (2017) Liver health in adults with Fontan circulation: a multicenter cross-sectional study. J Thorac Cardiovasc Surg 153:656–664

    Article  CAS  Google Scholar 

  29. 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  31. Wells ML, Fenstad ER, Poterucha JT et al (2016) Imaging findings of congestive hepatopathy. Radiographics 36:1024–1037

    Article  Google Scholar 

  32. 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  Google Scholar 

  33. Schuppan D, Afdhal NH (2008) Liver cirrhosis. Lancet 371:838–851

    Article  CAS  Google Scholar 

  34. Téllez L, Rodríguez 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

    Article  Google Scholar 

  35. Bryant T, Ahmad Z, Millward-Sadler H et al (2011) Arterialised hepatic nodules in the Fontan circulation: hepatico-cardiac interactions. Int J Cardiol 151:268–272

    Article  Google Scholar 

  36. 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

    Article  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Rathgeber SL, Harris KC (2019) Fontan-associated liver disease: evidence for early surveillance of liver health in pediatric Fontan patients. Can J Cardiol 35:217–220

    Article  Google Scholar 

  39. Hilscher MB, Johnson JN, Cetta F et al (2017) Surveillance for liver complications after the Fontan procedure. Congenit Heart Dis 12:124–132

    Article  Google Scholar 

  40. van Nieuwenhuizen RC, Peters M, Lubbers LJ et al (1999) Abnormalities in liver function and coagulation profile following the Fontan procedure. Heart 82:40–46

    Article  Google Scholar 

  41. Yang HK, Jang H-J, Khalili K et al (2020) CT and MR imaging findings of the livers in adults with Fontan palliation: an observational study. Abdom Radiol (NY) 45:188–202

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Ontasian Imaging Lab for administrative and statistical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Navallas.

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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 15 KB)

Supplementary file2 (DOCX 19 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Navallas, M., Yoo, SJ., Chavhan, G.B. et al. Semiquantitative characterization of dynamic magnetic resonance perfusion of the liver in pediatric Fontan patients. Pediatr Radiol 52, 483–492 (2022). https://doi.org/10.1007/s00247-021-05221-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00247-021-05221-6

Keywords

Navigation