Keywords
Arterial communicating arcades - embolization - gall bladder carcinoma - hepatic artery
- liver transplantation - pseudoaneurysm
Introduction
Interlobar arterial communication or communicating arcades (CA) in the hepatic hilum
have been recognized as one of the most important collateral pathways to the liver.
CAs play an important role in the blood supply to the caudate lobe and also have a
close relationship with the blood supply to the hilar biliary tract. Hepatic arterial
communicating arcades develop in hilum when either right or left hepatic artery is
occluded or significantly stenosed.[[1],[2]] If proper hepatic artery (PHA) is occluded, liver perfusion can occur through small
collaterals in the hepatic ligaments, collaterals around the common bile duct, inferior
phrenic artery, pancreatico-duodenal artery and intercalary “de novo” collaterals.[[3],[4]] We describe 3 cases showing the importance of hepatic arterial CA in endovascular
treatment of mycotic hepatic artery pseudoaneurysms (HAPAs), lobar arterial stenosis
following pediatric deceased donor liver transplant and locally advanced carcinoma
gallbladder infiltrating the right hepatic artery (RHA).
Case Series
Case 1
A 49-year-old lady presented with cholelithiasis and choledocholithiasis. After multiple
failed attempts of endoscopic management, the patient underwent a Roux-en-Y hepaticojejunostomy.
On post-operative day 5, the patient had low grade fever and elevated white cell count
(13,000/mm3). Ultrasound examination revealed a small collection anterior to the hepaticojejunostomy
site. No biliary dilatation was seen. A contrast enhanced CT (CECT) scan was performed
which revealed two extra hepatic pseudoaneurysms in the RHA proximal to its bifurcation
[[Figure 1A]]. Interventional radiologist was unavailable on that particular week. Drain was
placed by diagnostic radiologist avoiding injury to pseudoaneurysms at least to drain
the collection. Initially, bile stained fluid was drained, which was followed by drainage
of frank blood through the drain tube and hemodynamic instability of the patient.
Immediately patient was resuscitated and taken to angiosuite for embolization. In
view of the emergency situation, the in-house cardiologists performed the embolization.
CHA angiogram confirmed the presence of two irregularly filling extra hepatic RHA
pseudoaneurysms. A single coil was placed in the right hepatic artery proximal to
the pseudoaneurysms. Post coiling, RHA went into spasm and no reperfusion of pseudoaneurysm
was observed [[Figure 1B]]. However, on proper hepatic artery angiogram collateral supply from middle hepatic
artery (MHA) to distal RHA branches was observed [[Figure 1C]]. No reperfusion of pseudoaneurysms was observed post coiling, and the procedure
was concluded. Post procedure CECT scan done after two days did not reveal reperfusion
of pseudoaneurysms, however distal migration of coil in in RHA was noted [[Figure 1D]]. Post embolization, liver enzymes, and bilirubin were elevated (AST, ALT and ALP
were 1352, 1454, and 584, respectively, bilirubin was 2.3 mg/dl) on day 1 and become
near normal on day 7. Patient was discharged on 12th post embolization day. On 17th
post embolization day, the patient suddenly collapsed at home. She was found to be
hypotensive and resuscitated at a local hospital before being shifted back to our
hospital for management. Reperfusion of pseudoaneurysms and mild hemoperitoneum was
observed on repeat CECT scan [[Figure 1E]]. Angioembolization was performed by an interventional radiologist. Selective RHA
angiogram was performed [[Figure 1F]] and pseudoaneurysms were delineated. During embolization, attempt was not made
to cross the pseudoaneurysms in view of coil migration and rupture of aneurysms. RHA
was embolized with multiple 6 mm, 8 mm 0.018” micro coils. Middle hepatic artery (MHA)
was arising from proximal GDA. MHA angiogram showed faint perfusion of pseudoaneurysms
through intrahepatic arterial arcades [[Figure 1G]]. Intrahepatic arterial arcades were embolized with gelfaom particles and main trunk
of MHA was embolized with 5 mm 0.018” coils [[Figure 1H]]. Left hepatic artery (LHA) angiogram did not reveal perfusion of pseudoaneurysms;
however, few tiny CA were seen supplying the segment 4 of liver. Post embolization,
the patient recovered well. No significant increase in liver enzymes or bilirubin
was noted. No recurrence of pseudoaneurysm or other symptoms were observed on 12 months
follow up.
Figure 1 (A-H): A 49-year-old female patient, post hepaticojejunostomy presented with prehepatic
collection, fever and elevated total white cell count on day 5. Case describes CAs
from both middle and left hepatic arteries. (A) Arterial phase contrast enhanced CT
scan, oblique coronal MIP image showing two small mycotic pseudoaneurysms in (white
arrow) right hepatic artery. Small biliary collection was also noted. (B and C) Celiac
angiography digital image post embolization of right hepatic artery (by cardiologist
because of non-availability of Interventional radiologist) showing single coil (black
arrow) in RHA with non opacification of pseudoaneurysms and intrahepatic arterial
arcades communicating between right and accessory RHA (Black arrows). Pigtail catheter
placed in view to drain the collection caused rupture of pseudoaneurysm. (D) Arterial
phase contrast enhanced CT scan done post embolization day 2 revealed thrombosed pseudoaneurysm
and distally migrated crumpled coil (arrow) near RHA bifurcation. Arrow head shows
HepJ anastomotic bowel staple suture (E) Arterial phase contrast enhanced CT scan
done post embolization on post op day 17, MIP image shows reperfusion of pseudoaneurysms
(arrows) with increase in size of postero-medial pseudoaneurysm. (F) Digital right
hepatic artery angiogram showing migrated coil and two pseudoaneurysms (arrow). (G)
Post RHA coiling digital angiogram of MHA showing multiple intrahepatic arterial arcades
(small black arrows) feeding distal right hepatic artery. (H) Post MHA coiling, celiac
axis digital angiogram showing patent left HA (black arrow) and GDA
Case 2
A 9-year-old male patient, a known case of Alagille syndrome had undergone deceased
donor liver transplantation (DDLT). During transplant two arterial anastomosis were
performed. Right and left hepatic arteries of donor were anastomosed to recipient’s
PHA. Intraoperative color and spectral doppler ultrasound didn’t reveal any significant
abnormality in peak systolic velocity (PSV), resistive index (RI), and spectral waveform
of intrahepatic portions of right, segment 4 and left hepatic arteries. From 2nd post-operative
day, ultrasound revealed multiple subcapsular ischemic areas in right lobe of liver
and increasing post anastomotic (choledocho-choledochostomy) biliary dilatation. Color
and spectral doppler ultrasound revealed low RI (0.523 in RHA and 0.429 in segment
4 artery) and normal PSV in intraparenchymal portions of both right and left hepatic
arteries [[Figure 2A]-[C]]. Marginal alterations in liver enzymes were observed with normal INR and serum
lactate levels. In view of isolated right lobe subcapsular ischemic areas and biliary
dilatation, CECT scan was performed. CECT scan showed, short segment complete stenosis
of anastomotic and post anastomotic RHA and reperfusion of distal parenchymal arteries
through CA from segment 4 artery. Segment 4 artery and LHA were enhancing normally.
Multiple non enhancing subcapsular ischemic areas were seen in right lobe. No focal
abnormality seen in left lobe of liver. Mild biliary dilatation was seen [[Figure 2D]-[F]]. ERCP was done and plastic biliary stent was placed to assist biliary drainage.
Routine interval ultrasound follow was done till discharge. The patient is doing well
10 months after the transplant.
Figure 2 (A-F): A 8-year-old male patient, post liver transplant status with mild elevated liver
enzymes. (A and B) Spectral Doppler imaging of right and segment 4 hepatic arteries
showing elevated peak systolic velocity with low RI. (C) Gray scale and color Doppler
ultrasound image dual window showing biliary dilatation black arrow) with narrowing
at anastamotic site. (D and E) Arterial phase contrast enhanced CT scan coronal MIP
image showing post anastomotic unopacified proximal right hepatic artery (arrow heads).
Coronal and axial MIP image showing intrahepatic arterial arcades (small white arrows)
communicating between segment 4 artery and right hepatic artery. (F) Venous phase
CECT axial images showing multiple non enhancing subcapsular hypodense areas in right
lobe (open arrows) and predominant central biliary dilatation
Case 3
A 64-year-old male presented with progressive jaundice of 3 months duration. Total
bilirubin was 13 mg/dL. Transabdominal ultrasound revealed gall bladder (GB) fossa
mass with infiltration of adjacent liver and few hypoechoic lesions seen in right
lobe of liver. Hilar biliary confluence was involved with significant dilatation of
intra hepatic biliary radicles. Through ERCP, plastic biliary stent was placed in
to left side biliary ducts. Total bilirubin level came down to 3.5 mg/dL in 3 days.
The CECT scan revealed a large enhancing mass in GB fossa with infiltration of adjacent
liver. Few peripherally enhancing focal lesions were seen in right lobe of liver [[Figure 3A]]. Tumor was seen encasing the proximal RHA with its significant stenosis. Reperfusion
of Intraparenchymal RHA branches were observed through arterial CAs from left hepatic
artery both from segment 2/3 and segment 4 hepatic arteries [[Figure 3B] and [C]]. Spectral doppler ultrasound revealed significant stenosis of proximal RHA with
increased peak systolic velocity [[Figure 3D]-[F]]. Portal vein was not involved. Tumor was invading the biliary confluence with significant
bilateral intra hepatic biliary dilatation. Plastic biliary stent was seen in left
lobe biliary duct. Adenocarcinoma of gall bladder was confirmed on percutaneous biopsy
of GB fossa mass. Biopsy of right lobe liver lesions revealed cholangitic abscess.
The patient was informed about the prognosis and two self-expandable metallic stents
were placed.
Figure 3 (A-F): A 64-year-old male patient, inoperable case of GB fossa mass, presented with progressive
jaundice and abdominal pain since 3 months. Case describes CAs from both the branches
of left hepatic artery (segment 4 artery and segment 2/3 branches). (A) Venous phase
CT scan, coronal image showing ill-defined enhancing mass in segment 5 and GB fossa.
Rim enhancing lesion in segment VI. (B and C) Arterial phase contrast enhanced CT
scan, coronal MIP images showing arterial arcades (small arrows) communicating between
LHA (open white arrow) and RHA (Long arrow) and segment 4 artery (thick arrow) and
RHA respectively. Significant stenosis of proximal RHA seen (curved arrow). (D and
E) Spectral Doppler images showing normal velocity and low RI in intrahepatic branches
of RHA and high velocity and normal RI in segment IV artery. (F) Spectral Doppler
performed at stenotic proximal RHA showing increased peak systolic velocity (158 cm/sec)
with normal RI
Discussion
Inter lobar hepatic arterial communications or communicating arcades (CAs) develop
depending on the site of stenosis or occlusion of the hepatic artery. Interlobar collateral
vessels usually develop in the hepatic hilum in patients with interruption of either
right or left hepatic artery. These vessels are not visualized on angiograms in patients
with intact hepatic arterial supply.[[5]]
The CAs are located extrahepatically in the hepatic hilum or cranial to the portal
bifurcation close to the hilar bile duct. Caudate lobe is believed to derive its blood
supply not only from the segment I artery but also from the CA, because of which transarterial
chemoembolization for caudate lobe hepatocellular carcinoma is not very effective.[[1]]
Tohma et al. classified CAs in to type 1a, 1b, and 2 if arising from middle hepatic
artery, segment 4 artery and left hepatic artery respectively. Authors have also classified
CAs arising from right anterior hepatic artery, right hepatic artery or both as type
1, 2, and 3 respectively. In the present article we have presented all 3 cases with
CAs arising from left side. In first case CA was arising from middle hepatic artery
(type 1a). However, in after embolizing segment 4 artery we were able to see tiny
collaterals from left hepatic artery supplying the segment 4 area. So, this type of
collaterals from both middle and left hepatic artery is not mentioned in literature.
In second case of post liver transplant CA was from segment 4 hepatic artery (type
1b). In third case CA was arising from both the branches of left hepatic artery (segment
4 artery and segment 2/3 branches). Our first and third cases definitely add new types
to Toham et al. classification of CAs arising from left arteries and can be extended
as type 3a and 3b, respectively
Hepatic artery is the second most common site for visceral artery pseudoaneurysm after
splenic artery. Hepatic artery pseudoaneurysms (HAPAs) are usually iatrogenic and
can present as life threatening complications of hepatic, biliary, and pancreatic
interventions. Hepatic procedures accounts for 65% of these cases. Biliary and pancreatic
procedures accounts for 30% and 5%, respectively.[[6]] HAPAs can also be associated with intra-abdominal inflammation, infection, or trauma.[[6]] In our first case, surgery was uneventful and patient developed an infected biliary
collection near hepatico-jejunostomy site on post operation day 5. All the authors
felt right HAPAs were likely caused by infection (Klebsiella aerogenes bacteria) rather
iatrogenic, as patient recovered well after endovascular reintervention.
Coil embolization or exclusion of the pseudoaneurysms by stent graft is most effective
treatment option in an emergency setting, especially when associated with an infection.
Both proximal and distal ends of the parent arteries of the aneurysm must be embolized
simultaneously to block off the pseudoaneurysm in an extra hepatic HAPA, while proximal
embolization alone can be performed for an intrahepatic arterial aneurysm; however,
reestablishment of collateral circulation increases the risk of re-rupture of the
aneurysms.[[7]] In our case extra parenchymal right HAPAs were seen, which were initially embolized
by proximal solitary coil occlusion; however the coil migrated, pseudo-aneurysms were
re-perfused and bled again. Later successful embolization was performed by an interventional
radiologist with multiple coils in RHA, gel foam in CAs and coil in middle hepatic
artery.
Early (<1 month) arterial complications are associated with graft loss and a high
mortality rate after orthotropic liver transplant (OLT). Hepatic artery stenosis (HAS)
and hepatic artery thrombosis (HAT) are the most common hepatic arterial complications,
with high rates of morbidity and mortality. Untreated significant HA anastomotic strictures
can progress to HAT (65% at 6 months follow up). HAS is less frequently associated
biliary complications compared to HAT. Biliary complications can be seen up to 67%
in liver transplant recipients with HAS. Reduction of arterial flow during liver transplant
is commonly associated with biliary tree complications due to ischemic processes.
In some cases, HAS is likely to stimulate the development of arterial collaterals
that protect the liver from ischemia at the time of HAT.[[8]]
Doppler ultrasound (DUS) is the gold standard investigation to assess hepatic artery
patency in cases of HAT with sensitivity up to 92% or an increased resistive index
(RI). Anatomical defects (stenosis or kinking) can be detected by CT angiogram or
conventional angiography with a high sensitivity and specificity. Early HAS can be
detected by DUS with a sensitivity of 100%, a specificity of 99.5%, a positive predictive
value of 95% and a negative predictive value of 100%, and an overall accuracy of 99.5%.
However, MDCTA and standard angiography are the gold standard for HAS diagnosis.[[8]]
Biliary tract ischemia contributes to biliary strictures and anastomotic leakage in
liver transplants and can be seen up to 34% of patients. Division of the CA during
graft donation may potentially lead to biliary ischemia and complications. Thus, during
graft donation the right or left hepatic artery should not be dissected and separated
from the bile duct distally to prevent biliary ischemia.[[1]] In our second case anastomotic stenosis of RHA has led to development of anastamotic
biliary stricture (choledocho-choledochostomy) and visible biliary dilatation from
3rd day.
The third case is an uncommon presentation of gallbladder carcinoma involving the
right hepatic artery with development of visible hepatic arterial arcades on CECT
scan. Primary gallbladder carcinoma is the most common malignancy of the biliary tract.
The most common route of dissemination is direct invasion of the liver. Hepatic invasion
or hepatic metastasis has been reported in as many as 30%–80% of cases of gallbladder
carcinoma. Gall bladder malignancies with vascular invasion (main portal vein or hepatic
artery) are typically not amenable to surgery.[[9]]
In conclusion, first attempt of intervention failed in first case due to hepatic inter
arterial communication and incomplete embolization, which was later successfully embolized
by an Interventional radiologist. Percutaneous drain must be placed only after treating
pseudoaneurysms. In second case of post liver transplantation, arterial complication
was precisely detected on CECT and not on Doppler ultrasound. Right lobe of graft
survived because of hepatic inter arterial communications and no intervention was
required; however, patient developed few peripheral subcapsular ischemic changes in
right lobe and low-grade biliary dilatation which was managed by endoscopic plastic
stenting. With our first and third case, we describe new type of arterial communicating
arcades arising from middle hepatic artery (from GDA) and left hepatic artery. Thus,
knowledge of hepatic inter lobar arterial communication is important while treating
and diagnosing arterial diseases of both native and transplant liver.
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