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Multi-modality Imaging of Liver Transplant: ​ What you cannot afford to miss​

Multi-modality Imaging of Liver Transplant: ​ What you cannot afford to miss​

Elliot K. Fishman M.D.
Johns Hopkins Hospital

 

Objectives

  • Emphasize liver transplant complications that will affect the survival and health of the graft and the patient. ​
  • Identify pathologies in the pre-transplant evaluation that are critical for surgical planning.​
  • Review findings of early and delayed vascular and biliary complications with illustrative cases.  ​
  • Explain role for multi-modality imaging correlation and laboratory correlation. ​
Imaging of Liver Transplants

 

Post-transplant Ultrasound Assessment Practical Points

  • US is often the initial imaging modality for liver transplant grafts.
  • Include color and spectral doppler of all vessels, including peak systolic and end diastolic velocities of the arteries and calculation of the resistive index.
  • Image hepatic artery at porta hepatis and within liver.
  • Review the surgical note for the vascular and biliary anastomoses.
Example operative note describing the vascular and biliary anastomosis.

Example operative note describing the vascular and biliary anastomosis.

 

Hepatic Artery Normal Appearance in OLT

Surgical anastomosis:
  • Classic end-to-end anastomosis: do not confuse normal “fish mouth” anastomosis or Carrel patch with pseudoaneurysm
  • If celiac artery or proximal hepatic artery disease, then aorto-iliac conduit
  • Variant hepatic arterial anatomy may require multiple arterial anastomoses in living donor transplants. Each arterial anastomosis is susceptible to complications.
Normal doppler:
  • Low resistance (RI 0.55-0.8) with continuous diastolic flow
  • Sharp upstroke, with acceleration time <0.08 seconds
Hepatic Artery Normal Appearance in OLT

 

Hepatic Artery Normal Appearance in OLT

Surgical anastomosis:
  • Classic end-to-end anastomosis: do not confuse normal “fish mouth” anastomosis or Carrel patch with pseudoaneurysm
  • If celiac artery or proximal hepatic artery disease, then aorto-iliac conduit
  • Variant hepatic arterial anatomy may require multiple arterial anastomoses in living donor transplants. Each arterial anastomosis is susceptible to complications.
Normal doppler:
  • Low resistance (RI 0.55-0.8) with continuous diastolic flow
  • Sharp upstroke, with acceleration time <0.08 seconds
Hepatic Artery Normal Appearance in OLT

 

Hepatic Artery Normal Appearance in OLT

Surgical anastomosis:
  • Classic end-to-end anastomosis: do not confuse normal “fish mouth” anastomosis or Carrel patch with pseudoaneurysm
  • If celiac artery or proximal hepatic artery disease, then aorto-iliac conduit
  • Variant hepatic arterial anatomy may require multiple arterial anastomoses in living donor transplants. Each arterial anastomosis is susceptible to complications.
Normal doppler:
  • Low resistance (RI 0.55-0.8) with continuous diastolic flow
  • Sharp upstroke, with acceleration time <0.08 seconds
Hepatic Artery Normal Appearance in OLT

 

Case: Transient Elevated RI

Transient Elevated RI (>0.8) is a common benign finding in the first 4 days post-transplant. RIs should be followed until normalization.

Contrast-enhanced ultrasound is excellent to confirm patency of the hepatic artery and may be performed at the bedside. There is emerging data on the use of Superb Microvascular Imaging ultrasound technique to evaluate low-flow vessels.

Garcia-Criado, 2009; Güven, 2019

Case: Transient Elevated RI

 

Case: Early Hepatic Artery Thrombosis

Clinical follow-up: On post-op day 14, patient underwent new liver transplant. The liver explant demonstrated hepatic artery thrombosis with ischemic injury and necrosis.

Hepatic artery thrombosis is the most common vascular complication.

Loss of flow on ultrasound is diagnostic of an hepatic artery thrombosis. Doppler US has nearly 100% sensitivity for early (<1 week post-op) hepatic artery thrombosis.

There is a progression of ultrasound findings in impending hepatic arterial thrombosis:
decreased diastolic flow (elevated RI). → blunting of systolic upstroke and parvus tardus wave form (decreased RI) → loss of flow

Bhargava, 2011; Sannananja, 2018; Horrow, 2007, ; Vaidya, 2007

Case: Early Hepatic Artery Thrombosis

 

Case: Early Hepatic Artery Thrombosis

2 weeks post-op: Markedly elevated liver function tests found on routine follow-up. US shows abnormal low RI in the HA at the porta hepatis, no flow more centrally and focal hepatic infarct. CT confirms HA thrombosis and hepatic infarct.

Clinical follow-up: Patient required repeat OLT 4 days later. Pathology of the liver explant showed massive panlobular hepatocyte necrosis and bile duct loss consistent with hepatic artery occlusion.

Biliary ischemia is a primary concern in hepatic artery disease because the bile ducts are solely supplied by the arterial system. Complications can be bilomas, biliary leaks, and biliary strictures. There are variable complications after early hepatic arterial thrombosis, ranging from fulminant hepatic necrosis to self-limiting complications.

Hepatic infarcts can be readily visualized on ultrasound.

Bhargava, 2011; Sannananja, 2018; Horrow, 2007, ; Vaidya, 2007

Case: Early Hepatic Artery Thrombosis

 

Case: Late Hepatic Artery Thrombosis

Clinical follow-up: graft survived with recurrent liver abscesses for 6 years.

Rising liver function tests may be the first indication that something is wrong with the hepatic graft.

Bhargava, 2011; Sannananja, 2018; Horrow, 2007, ; Vaidya, 2007

Case: Late Hepatic Artery Thrombosis

 

Case: Late Hepatic Artery Thrombosis

1 month after liver transplant: low RI in hepatic artery although arterial flow is present. Extensive collateral arteries on angiography. Hepatic infarct seen on CT. 

Ultrasound is less sensitive for the detection of late hepatic arterial thrombosis (>1 week post-op) due to the formation of collateral vessels.

Outcomes of late hepatic arterial thrombosis are not as severe as early thrombosis because of the formation of collateral vessels.

Differential diagnosis of low RI:
  • Late hepatic artery thrombosis with collateral vessels
  • Hepatic artery stenosis
  • Celiac artery stenosis
Bhargava, 2011; Sannananja, 2018; Horrow, 2007, ; Vaidya, 2007

Case: Late Hepatic Artery Thrombosis

 

Case: Hepatic Artery Thrombosis

Intrahepatic collection on CT and US. RI in the hepatic artery is normal. Hepatic artery occlusion on angiogram.

Intrahepatic collections may be due to underlying hepatic artery thrombosis, even in the setting of normal hepatic artery RI, because RI may be preserved in late hepatic artery thrombosis.

Bhargava, 2011; Sannananja, 2018; Horrow, 2007, ; Vaidya, 2007

Case: Hepatic Artery Thrombosis

 

Case: Hepatic Artery Stenosis

Low RI necessitates evaluation of the hepatic artery to look for a more proximal hepatic artery stenosis or thrombosis.

US findings:
  • Distal to stenosis: RI < 0.5, parvus tardus (acceleration time <0.08 sec).
  • At the stenosis: vessel narrowing, peak systolic velocity >200cm/s
Bhargava, 2011; Garcia-Criado, 2009

Case: Hepatic Artery Stenosis

 

Case: Hepatic Artery Stenosis

Severe hepatic artery stenosis may cause graft ischemia, although most mild stenosis only causes mild graft dysfunction.

If there is a low RI in the hepatic artery, but the proximal artery cannot be followed with ultrasound, then it must be evaluated on another modality.

Differential diagnosis of low RI in the intrahepatic arteries:
  • hepatic artery stenosis
  • late hepatic artery thrombosis with collateral vessels.
  • celiac axis stenosis
Bhargava, 2011; Garcia-Criado, 2009

Case: Hepatic Artery Stenosis

 

Case: Celiac Artery Stenosis

Celiac axis stenosis may be graft-threatening if not recognized pre-operatively. The celiac artery, SMA, and variant arterial anatomy should always be addressed in the pre-transplant imaging exam.

Celiac axis stenosis is often asymptomatic pre-operatively because of retrograde collateral flow from the SMA. After transplant, the graft is entirely dependent on arterial flow from the celiac axis because of surgical division of collaterals.

Suspect celiac artery stenosis if the post-operative RI is decreased but there is no hepatic arterial thrombosis or stenosis.

Horrow, 2020

Case: Celiac Artery Stenosis

 

Case: Splenic Steal Syndrome

Splenic steal syndrome presents as abnormal LFTs, splenomegaly, ascites, and thrombocytopenia.

It is due to increased flow in the splenic artery away from the hepatic graft, causing graft hypoperfusion. Steal syndrome has also been reported with the gastroduodenal artery.

Imaging findings:
  • Low PSV in the hepatic artery (<35cm/s)
  • Abnormal RI in the hepatic artery
  • Dilated splenic artery: diameter >4mm, or >6mm larger than hepatic artery
  • Splenomegaly (>829cc)
Li, 2017; Horrow, 2020

Case: Splenic Steal Syndrome

 

Case: Splenic Steal Syndrome

Low PSV in the hepatic artery (<35 cm/s) should prompt consideration of splenic steal syndrome.

Definitive diagnosis is with conventional angiography. Treatment is splenic artery embolization.

Li, 2017; Horrow, 2020

Case: Splenic Steal Syndrome

 

Case: Hepatic Artery Pseudoaneurysm

Hepatic artery pseudoaneurysms are rare complications.

Extrahepatic pseudoaneurysms are more common and tend to occur at the site of anastomosis or angioplasty, and are often mycotic. Intrahepatic pseudoaneurysms are less likely and tend to occur at the site of graft biopsy or focal infection.

Vascular intervention is required to avoid complications such as rupture, or fistulization with the biliary or gastrointestinal tracts.

Garcia-Criado, 2009; Kimura, 2020; Vaidya, 2007

Case: Hepatic Artery Pseudoaneurysm

 

Hepatic Arterial Complications Summary

Hepatic Arterial Complications Summary

 

Portal Vein Normal Appearance in OLT

Portal vein anastomosis in OLT
  • Typically end-to-end
  • Pre-existing portal vein thrombosis may require an interposition graft
Normal US appearance
  • Spectral wave form monophasic and hepatopetal
  • Small change in caliber at anastomosis, often echogenic with ring


Portal Vein Normal Appearance in OLT

 

Case: Portal Vein Thrombosis

Portal venous complications are less common the arterial complications. When they do occur, they typically occur at the anastomosis.

Risk factors for portal venous thrombosis:
  • hypercoagulable state
  • increased down stream resistance
  • decreased portal inflow, prior portal vein surgery (e.g. TIPS)
  • technical problems (e.g. significant differences in caliber of donor and recipient portal veins)
Kimura, 2020; Caiado, 2007

Case: Portal Vein Thrombosis

 

Case: Portal Vein Stenosis

Imaging findings of portal venous stenosis:
  • Focal narrowing at the portal vein
  • Stenosis-to-pre-stenosis PSV ratio >3:1
  • Portal vein PSV>125 cm/s
Kimura, 2020

Case: Portal Vein Stenosis

 

Hepatic Vein & IVC Normal Appearance in OLT

Multiple surgical techniques exist for the IVC anastomosis.
  • Most are currently performed using the piggyback technique.
Normal US appearance: Triphasic, antegrade

Bhargava,2011; Ahlawasi, 2012; Crossin, 2003

Hepatic Vein & IVC Normal Appearance in OLT

 

Hepatic Vein & IVC Normal Appearance in OLT

Normal US evaluation of the middle hepatic vein. Patient status post deceased donor transplant with side-to-side cavocavostomy.

Hepatic Vein & IVC Normal Appearance in OLT

 

Case: Hepatic Vein and IVC Thrombosis

IVC and hepatic venous complications are rare in OLT and can cause graft dysfunction or failure.

Post-transplant ultrasound should routinely evaluate both the hepatic veins as well as the piggyback anastomosis.

Kimura, 2020

Case: Hepatic Vein and IVC Thrombosis

 

Case: IVC Stenosis

Hepatic vein and IVC complications are more common in living donor transplants because of the more complex venous reconstruction.

Risk factors for hepatic vein/IVC stenosis:
  • Pediatric transplants, retransplantation, and split graft transplants
  • Size discrepancy between donor and recipient veins
  • Supracaval kinking
Imaging findings of stenosis:
  • Loss of normal cardiac pulsatility in hepatic vein
  • Pre-stenotic dilatation
  • Stenotic-to-pre-stenotic velocity ratio >3-4:1
  • If early post-op, look for fluid collection/hematoma from cavocaval dehiscence that may cause extrinsic compression of IVC
Kimura, 2020; Singh, 2010; Crossin, 2003

Case: IVC Stenosis

 

Case: Graft Torsion

Graft torsion may be a cause of hepatic venous outflow obstruction in living donor liver transplants. HV outflow obstruction is graft threatening because it causes significant parenchymal congestion which compromises arterial and portal inflow, as seen in this case with portal flow reversal.

Differential diagnosis for hepatic venous outflow obstruction in living donor liver transplant:
  • Graft torsion
  • Hepatic venous stenosis at the surgical anastomosis
  • Hepatic venous thrombosis
Repair of the surgical anastomosis is extensive, so it is important to consider torsion and graft repositioning first.

Treatment is surgical graft repositioning and hepatopexy.

Abdelaziz, 2016; Jeng, 2017

Case: Graft Torsion

 

Biliary Anastomosis in OLT

Biliary anastomosis
  • Typically end-to-end
  • Hepaticojejunostomy may be performed if underlying extrahepatic biliary disease (e.g. primary sclerosing cholangitis) or for technical reasons.
  • Cholecystectomy performed on implant
Bhargava,2011; Ahlawasi, 2012

Biliary Anastomosis in OLT

 

Case: Biliary Stones

Biliary stones tend to occur >1 year post-transplant, although are overall much less common than biliary strictures or leaks.

Biliary stones or sludge suggest underlying biliary stasis, which may be due to stricture. Biliary stones may also be medication-induced, such as with cyclosporine.

Biliary stones can cause obstruction and cholangitis and often require percutaneous, endoscopic, or surgical removal.

Crossin, 2003

Case: Biliary Stones

 

Case: Biliary Cast Syndrome

Biliary cast syndrome is due to biliary ischemia with sloughing of the biliary mucosa. It is usually due to underlying hepatic artery thrombosis or stenosis, therefore biliary casts on exam should prompt close evaluation of the hepatic artery.

Hu, 2016

Case: Biliary Cast Syndrome

 

Case: Biliary Cast Syndrome

Imaging findings:
  • Mild: bile ducts are subtle periportal branching structures isoechoic to liver
  • Severe: biliary ductal dilatation and strictures, echogenic or T1 hyperintense casts, bilomas
  • Filling defects on cholangiogram
Look for associated hepatic arterial pathology or proximal biliary stricture

Hu, 2016

Case: Biliary Cast Syndrome

 

Summary of Case Teaching Points

  • Biliary ischemia is a primary concern in hepatic arterial disease.
  • Progression of ultrasound findings in impending hepatic arterial thrombosis.
  • CE-US is excellent to evaluate the hepatic artery at the bedside
  • Low RI necessitates evaluation of the hepatic artery.
  • US is less sensitive for the diagnosis of late HA thrombosis due to collaterals
  • Rising LFTs may herald serious arterial complications.
  • Celiac artery should be evaluated on pre-transplant imaging.
  • Low PSV in the hepatic artery should prompt consideration of splenic steal syndrome.
  • HA pseudoaneurysm is rare but requires vascular intervention to prevent life-threatening complications.


Imaging of Liver TransplantsImaging of Liver Transplants

 

Summary of Case Teaching Points

Portal venous complications are uncommon.

Imaging of Liver Transplants Imaging of Liver Transplants

 

Summary of Case Teaching Points

  • Hepatic vein and IVC complications are more common in living donor liver transplants.
  • Graft torsion may cause hepatic venous outflow obstruction in LDLT.


Imaging of Liver Transplants Imaging of Liver Transplants

 

Summary of Case Teaching Points

  • Biliary stones suggest underlying cause of biliary stasis.
  • Biliary casts are due to biliary ischemia so should prompt close evaluation of the hepatic artery.


Imaging of Liver Transplants Imaging of Liver Transplants

 

Summary of Case Teaching Points

  • Hepatic vein and IVC complications are more common in living donor liver transplants.
  • Graft torsion may cause hepatic venous outflow obstruction in LDLT.
  • Biliary ischemia is a primary concern in hepatic arterial disease.
  • Progression of ultrasound findings in impending hepatic arterial thrombosis.
  • CE-US is excellent to evaluate the hepatic artery at the bedside
  • Low RI necessitates evaluation of the hepatic artery.
  • US is less sensitive for the diagnosis of late HA thrombosis due to collaterals
  • Rising LFTs may herald serious arterial complications.
  • Celiac artery should be evaluated on pre-transplant imaging.
  • Low PSV in the hepatic artery should prompt consideration of splenic steal syndrome.
  • HA pseudoaneurysm is rare but requires vascular intervention to prevent life-threatening complications.
  • Biliary stones suggest underlying cause of biliary stasis.
  • Biliary casts are due to biliary ischemia so should prompt close evaluation of the hepatic artery.
  • Portal venous complications are uncommon.


Imaging of Liver Transplants

 

References

  • Bhargava, Puneet, et al. "Imaging of orthotopic liver transplantation." American Journal of Roentgenology196.3_supplement (2011): WS15-WS25.
  • Horrow, Mindy M., et al. "Complications after Liver Transplant Related to Preexisting Conditions: Diagnosis, Treatment, and Prevention." RadioGraphics 40.3 (2020): 895-909.
  • Makowka, Leonard, et al. "Surgical technique of orthotopic liver transplantation." Gastroenterology Clinics of North America 17.1 (1988): 33.
  • García-Criado, Ángeles, et al. "Doppler ultrasound findings in the hepatic artery shortly after liver transplantation." American Journal of Roentgenology 193.1 (2009): 128-135.
  • Güven, Fadime, et al. "The Value of Superb Microvascular Imaging in Detecting Hepatic Artery Occlusion in Liver Transplantation: A Preliminary Study." Ultrasound quarterly35.4 (2019): 325-329.
  • Sannananja, Bhagya, et al. "Tricky findings in liver transplant imaging: a review of pitfalls with solutions." Current Problems in Diagnostic Radiology 47.3 (2018): 179-188.
  • Horrow, Mindy M., et al. "Sonographic diagnosis and outcome of hepatic artery thrombosis after orthotopic liver transplantation in adults." American Journal of Roentgenology189.2 (2007): 346-351.
  • Vaidya, Sandeep, et al. "Liver transplantation: vascular complications." Ultrasound quarterly 23.4 (2007): 239-253.
  • Horrow, Mindy M., et al. "Complications after Liver Transplant Related to Preexisting Conditions: Diagnosis, Treatment, and Prevention." RadioGraphics 40.3 (2020): 895-909.
  • Li, Chaolun, et al. "Current understanding and management of splenic steal syndrome after liver transplant: a systematic review." Transplantation Reviews 31.3 (2017): 188-192.
  • Kimura, Yukiyoshi, et al. "Liver Transplant Complications Radiologist Can't Miss." Cureus 12.6 (2020).
  • Makowka, Leonard, et al. "Surgical technique of orthotopic liver transplantation." Gastroenterology Clinics of North America 17.1 (1988): 33.
  • Caiado, Angela Hissae Motoyama, et al. "Complications of liver transplantation: multimodality imaging approach." Radiographics 27.5 (2007): 1401-1417.
  • Alhawsawi, Abdulelah M., and Juan del Rio Martin. "Surgical Techniques in Liver Transplantation." Liver Anesthesiology and Critical Care Medicine. Springer, New York, NY, 2012. 83-95.
  • Crossin, Jane D., Derek Muradali, and Stephanie R. Wilson. "US of liver transplants: normal and abnormal." Radiographics23.5 (2003): 1093-1114.
  • Hu, Bing, and Mindy M. Horrow. "Ultrasound of biliary cast syndrome and its mimics." Ultrasound quarterly 32.3 (2016): 258-270.
  • Singh, Ajay K., et al. "Postoperative imaging in liver transplantation: what radiologists should know." Radiographics30.2 (2010): 339-351.
  • Abdelaziz, Omar, and Hussein Attia. "Doppler ultrasonography in living donor liver transplantation recipients: Intra-and post-operative vascular complications." World journal of gastroenterology 22.27 (2016): 6145.
  • Jeng, Kuo-Shyang, et al. "Graft calcification caused by a torsion of the hepatic vein after a living-related donor liver transplantation." Annals of hepatology 16.1 (2017): 160-163.

 

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