The State of the Liver in the Adult Patient after Fontan Palliation

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1 The State of the Liver in the Adult Patient after Fontan Palliation Fred Wu, M.D. Boston Adult Congenital Heart Service Boston Children s Hospital/Brigham & Women s Hospital 7 th National Adult Congenital Heart Association Conference Chicago, Illinois September 5, 2014

2 Objectives To highlight the physiologic vulnerabilities of the liver in the Fontan circulation To review our current knowledge of liver disease and its clinical impact in patients with Fontan circulation To identify gaps in our current understanding of Fontan-related liver disease and to suggest directions for future study

3 The heart and liver disease

4 Potential sources of hepatic injury Pre-Fontan factors: Hypoxemia Heart failure Perioperative liver injury Factors resulting from Fontan physiology: Hepatic congestion Compromised cardiac output Comorbidities: Hepatitis C co-infection Hepatotoxic drugs

5 Hepatic circulation 30% from hepatic artery / 70% from portal vein Hepatic arterial buffer response allows reciprocal change in hepatic arterial flow when portal venous flow changes. Gelman et al. Anesthesiology 2004.

6 Hepatic microcirculation Blood flow within acini is directed radially from hepatic arterioles and portal venules into the central veins. Oxygen and nutrient content decrease as blood flows from zone 1 through zone 3. Zone 3 is most sensitive to injury from circulatory disturbances and byproducts of Jones AL. Hepatology: A Textbook of Liver Disease, 1996.

7 Fontan physiology Fontan operation results in: Systemic oxygen saturation and ventricular volume load restored to near normal levels Lower resting cardiac output and limited ability to augment cardiac output with stress Increased central venous pressure Gewillig et al. Interact Cardiovasc Thorac Surg 2010.

8 Hepatic blood flow in heart failure Despite compensatory mechanisms, patients with congestive heart failure have significantly decreased hepatic blood flow. Patients with congestive heart failure and clinical hypoxic hepatitis ( shock liver ) have even more profound decrease in hepatic blood flow. Henrion et al. Medicine 2003.

9 Fontan circulation and liver disease A 15-year-old girl was found to have severe liver fibrosis on liver biopsy at the time of cholecystectomy, 5 ½ years following a modified Fontan procedure

10 Gross pathologic changes Hepatomegaly Nodular liver surface Fibrosis Nutmeg liver appearance Masses (adenomas/hepatocellular carcinoma) Ghaferi et al. J Thorac Cardiovasc Surg 2005.

11 Sinusoidal dilation Hepatic fibrosis Centrilobular Portal Regenerative nodules Cardiac cirrhosis Histologic changes Harmon et al. 23rd International Symposium on Congenital Heart Disease in the Adult 2013.

12 Frequency of hepatic fibrosis 50 Portal fibrosis (n=67) 50 Sinusoidal fibrosis (n=63) % Stage Cirrhosis Stage Wu et al. AHA Scientific Sessions 2013.

13 Frequency of hepatic fibrosis 50 Portal fibrosis (n=67) 50 Sinusoidal fibrosis (n=63) % Stage Cirrhosis Stage Wu et al. AHA Scientific Sessions 2013.

14 Frequency of hepatic fibrosis 50 Portal fibrosis (n=67) 50 Sinusoidal fibrosis (n=63) % Stage Cirrhosis Stage Wu et al. AHA Scientific Sessions 2013.

15 Imaging findings Hepatosplenomegaly Nodular liver surface Heterogeneous contrast enhancement Portal hypertension (ascites, varices) Masses (arterialized nodules, hepatocellular carcinoma) Kiesewetter et al. Heart Bryant et al. Int J Cardiol 2010.

16 Frequency of imaging findings (n=54) % abnormal Heterogeneous enhancement (n=42) Segmental irregularity (n=53) Caudate-right lobe ratio >0.6 Irregular liver contour Splenomegaly (n=52) Ascites Collaterals/ Varices (n=53) Wu et al. AHA Scientific Sessions 2013.

17 Correlation between tests Imaging and liver histopathology (n=23) No correlation between number of abnormal imaging findings and sinusoidal or portal fibrosis stages. No correlation between presence of specific imaging findings and sinusoidal or portal fibrosis stages. Wu et al. AHA Scientific Sessions 2013.

18 Abnormal biochemical studies n % > ULN GGT (U/L) ALT/SGPT (U/L) Total bilirubin (mg/dl) AST/SGOT (U/L) Alkaline phosphatase (U/L) n % < LLN Platelets (K cells/µl) Albumin (g/dl) Wu et al. AHA Scientific Sessions 2013.

19 Abnormal hepatic function Elevated prothrombin time Reduced Factor V activity Increased galactose elimination half-life Narkewicz et al. J Pediatr Gastroenterol Nutr 2003.

20 Abnormal hepatic function Indocyanine green testing Abnormal disappearance and retention rates Similar to results in patients with viral cirrhosis Poor correlation with ELF score (TIMP-1, PIIINP, HA) Guha al. Int J Cardiol 2013.

21 Clinical impact of liver disease Histopathologic Features of the Liver in Patients with Fontan Palliation: A 21-Year Review 26 (38.2%) patients experienced an outcome: 4 heart transplants, 22 deaths Median age at death or transplant: 26.0y 13 of 22 deaths preceded by ascites, encephalopathy or variceal bleeding in the week prior to death Harmon et al. 23rd International Symposium on Congenital Heart Disease in the Adult 2013.

22 Clinical impact of liver disease n=73 (adult and pediatric) 50% 45% 40% 35% 30% 25% 20% 15% 10% 5% 0% Varices Ascites Splenomegaly Platelets < 150k Elder et al. Int J Cardiol 2013.

23 Clinical impact of liver disease Liver disease associated with major adverse events late after Fontan operation. Freedom from sudden death, HF death or transplant (%) MELD-XI > 18 Log rank p = MELD-XI < 11 MELD-XI Time since MELD-XI (years) Count (n) VAST Score <2 VAST Score 2 Features of Portal Hypertension Event Type HCC Transplant Death None Assenza et al. Heart 2013 Elder et al. IJC 2013

24 Clinical impact of liver disease Severity of histological fibrosis in Fontan physiology may not correlate with time until death or cardiac transplant. Harmon et al. 23rd International Symposium on Congenital Heart Disease in the Adult 2013.

25 Liver disease and mortality Liver cirrhosis in Fontan patients does not appear to affect one-year post-heart transplant mortality Simpson et al. J Heart Lung Transplant 2014

26 Reversal of liver disease?

27 Reversal of liver disease? Reversal of cirrhosis observed in 75 patients (49%) of 153 patients with baseline cirrhosis.

28 Reversal of liver disease? 51% with improvement in fibrosis stage. Proportion with bridging fibrosis or cirrhosis decreased from 38% to 12%.

29 Reversal of liver disease? Proportion with bridging fibrosis or cirrhosis decreased from 31% to 6%.

30 Reversal of liver disease? In 9 patients who underwent surgical biliary decompression without restenosis, fibrosis improved in 6 patients and remained unchanged in 3 patients.

31 Reversal of liver disease? In 87 patients, mean fibrosis score improved from 3.4 ± 0.2 to 2.6 ± 0.2 (p = ) over 63 ± 6 months. Fibrosis score improved in 53% and remained stable in 26%.

32 Conclusions Evidence of liver disease by some testing modality is nearly universal. Individual modalities for assessing liver health do not always correlate with patient outcomes or with one another. Best way to test for liver disease remains unknown but will likely require multi-faceted approach. Caution must be exercised when applying lessons learned from traditional models of liver disease.

33 Thank you, Chicago!

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