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.
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References
Cowgill LD (1991) The Fontan procedure: a historical review. Ann Thorac Surg 51:1026–1030
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
de Lange C (2020) Imaging of complications following Fontan circulation in children — diagnosis and surveillance. Pediatr Radiol 50:1333–1348
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
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
Khanna G, Bhalla S, Krishnamurthy R, Canter C (2012) Extracardiac complications of the Fontan circuit. Pediatr Radiol 42:233–241
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
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
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
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
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
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
Emamaullee J, Zaidi AN, Schiano T et al (2020) Fontan-associated liver disease: screening, management, and transplant considerations. Circulation 142:591–604
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
Egbe AC, Poterucha JT, Warnes CA et al (2018) Hepatocellular carcinoma after Fontan operation: multicenter case series. Circulation 138:746–748
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
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
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
Dillman JR, Trout AT, Alsaied T et al (2020) Imaging of Fontan-associated liver disease. Pediatr Radiol 50:1528–1541
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
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
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
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
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
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
Bloom S, Kemp W, Lubel J (2015) Portal hypertension: pathophysiology, diagnosis and management. Intern Med J 45:16–26
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
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
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
Wallihan DB, Podberesky DJ (2013) Hepatic pathology after Fontan palliation: spectrum of imaging findings. Pediatr Radiol 43:330–338
Wells ML, Fenstad ER, Poterucha JT et al (2016) Imaging findings of congestive hepatopathy. Radiographics 36:1024–1037
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
Schuppan D, Afdhal NH (2008) Liver cirrhosis. Lancet 371:838–851
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
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
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
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
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
Hilscher MB, Johnson JN, Cetta F et al (2017) Surveillance for liver complications after the Fontan procedure. Congenit Heart Dis 12:124–132
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
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
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The authors acknowledge the Ontasian Imaging Lab for administrative and statistical support.
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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
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DOI: https://doi.org/10.1007/s00247-021-05221-6