Primary and secondary malignancies in the liver present one of
the most challenging problems in clinical oncology.
Colorectal cancer is the second leading cause of cancer-related
death in the United States, with liver metastases accounting for
about half of these deaths. Other tumors that frequently develop
fatal hepatic metastases-despite a resectable primary tumor-include
ocular melanoma, neuroendocrine tumors, and gastrointestinal
sarcomas. Hepatocellular carcinoma (hepatoma) is the most common
fatal malignancy worldwide, killing 1.25 million people
Less than half of patients with metastatic colorectal cancer
respond to systemic chemotherapy, and the survival benefit is no
more than several months. Hepatoma has very little response to
systemic therapy. External beam radiotherapy is limited by the
radiosensitivity of the liver. Novel approaches for treating
hepatic malignancies include direct infusion of chemotherapeutic
drugs into the hepatic artery or portal vein, em-bolization,
percutaneous ablation with various physical and chemical agents,
and interstitial or intravascular injection of radioactive agents.
These techniques have in common a regional or local approach to
Chemoembolization combines hepatic artery embolization with
simultaneous infusion of a concentrated dose of chemotherapeutic
drugs. There are several theoretical advantages to this technique.
First, embolization renders the tumor ischemic, depriving it of
nutrients and oxygen. Second, tumor drug concentrations are 1 to 2
orders of magnitude higher than are achieved by infusion alone.1,2
Third, because blood flow is arrested, the dwell time of the
chemotherapy is markedly prolonged, with measurable drug levels
present as long as a month later.3,4 Fourth, the ischemia induced
by embolization helps to overcome drug resistance by causing
metabolically active cell membrane pumps to fail, thereby
increasing intracellular retention of the chemotherapeutic drug.5
Finally, because most of the drug is retained in the liver,
systemic toxicity is reduced.6
Patient selection for chemoembolization
Patients selected for regional therapy must have their tumor
confined to the liver. Patients with minimal or indolent
extrahepatic disease may be candidates if the liver disease is
considered the dominant source of morbidity and mortality for that
Tolerance of hepatic artery occlusion is dependent upon the
presence of portal vein inflow. Compromise in portal venous blood
flow is a relative contraindication to hepatic embolization.
Chemoembolization can be performed safely despite portal vein tumor
thrombus if hepatopetal collateral flow is present.7 In this
setting, a smaller volume of the liver should be embolized at any
When the parenchyma is diseased, the liver becomes more
dependent on the hepatic artery for its blood supply. A subgroup of
patients has been identified who are at high risk of acute hepatic
failure following hepatic artery embolization. They have a
constellation of >50% of the liver volume replaced by tumor,
lactate dehydrogenase (LDH) >425 IU/L, aspartate
aminotransferase (AST) >100 IU/L, and total bilirubin 32 mg/dl.8
The presence of hepatic encephalopathy or jaundice are absolute
contraindications to embolization.
Biliary obstruction is also a contraindication. Even with a
normal serum bilirubin, the presence of dilated intrahepatic bile
ducts places the patient at high risk for biliary necrosis of the
obstructed segment(s) of the liver.
Procedure and peri-procedural care
Pretreatment assessment-Preoperative evaluation for
chemoembolization includes a tissue diagnosis; cross-sectional
imaging of the liver; exclusion of extrahepatic disease; and
laboratory studies, including complete blood count, prothrombin
time, partial thromboplastin time, creatinine level, liver function
tests, and tumor markers.
Patient education-Before em-barking on this fairly arduous
palliative regimen, patients should be thoroughly informed of the
side effects and risks. Up to 80% to 90% of patients suffer from
postembolization syndrome, characterized by pain, fever, and nausea
and vomiting. The severity of these symptoms varies tremendously
from patient to patient, and can last from a few hours to several
days. Other significant toxicities are rare. Serious complications
occur after 5% to 7% of procedures (see below). Given the
significant discomforts, hazards, and expense of this treatment,
its palliative role should be clearly understood.
Procedure-Patients must fast overnight, and are admitted to the
hospital the morning of the procedure. A Foley catheter is
inserted, and vigorous hydration is initiated (normal saline
solution [NSS] at 200 to 300 mL/hr). Prophylactic antibiotics
(cephazolin 1 gram, metronidazole 500 mg) and antiemetics
(odansetron 24 mg, decadron 10 mg, diphenhydramine 50 mg) are
administered intravenously. The benefit of antibiotic prophylaxis
Diagnostic visceral arteriography is performed to determine the
arterial supply to the liver and confirm patency of the portal
vein. The origins of vessels supplying the gut, particularly the
right gastric and supraduodenal arteries, are carefully noted in
order to avoid embolization of the stomach or small bowel.
Once the arterial anatomy is understood clearly, a catheter is
advanced superselectively into the right or left hepatic artery,
depending upon which lobe holds the most tumor (figure 1). The
chemoembolic mixture is injected until nearly complete stasis of
blood flow is achieved (figure 2). In our institution, we use 100
to 150 mg cisplatin, 50 mg doxorubicin, and 10 mg mitomycin-C
dissolved in 10 mL of radiographic contrast and emulsified with 10
mL of iodized oil and 150 to 250 µm polyvinyl alcohol (PVA)
particles. The patient receives intra-arterial lidocaine (30 mg
boluses up to 200 mg total) and intravenous narcotics to alleviate
pain during the embolization. After the procedure, vigorous
hydration (NSS 3L/24 hr), intravenous antibiotics, and antiemetic
therapy (odansetron and decadron) are continued. Narcotics,
perchlorpromazine, and acetominophen are supplied liberally for
control of pain, nausea, and fever. The patient is discharged as
soon as oral intake is adequate and parenteral narcotics are not
required for pain control. About half of patients are discharged in
1 day, most in 2 days. Oral antibiotics are continued for another 5
days, as well as antiemetics and oral narcotics if needed. The
patient returns for a second procedure directed at the other lobe
of the liver 3 to 4 weeks later. Depending upon the arterial
anatomy, two to four procedures are required to treat the entire
liver, after which response is assessed by repeat imaging studies
and tumor markers.
Complications-Major complications of hepatic embolization
include hepatic insufficiency or infarction, hepatic abscess, tumor
rupture, surgical cholecystitis, and non-target em-bolization to
the gut. With careful patient selection and scrupulous technique,
the collective incidence of these serious events is 3% to 4%. Other
complications include periprocedural cardiac events, renal
insufficiency, and anemia requiring transfusion, with incidences of
<1% each. Thirty-day mortality ranges from 1% to 4%.
Results in specific diseases
Hepatoma-Among combined series of 800 patients with unresectable
hepatocellular carcinoma treated palliatively with
chemoembolization in Asia, Europe, and in the United States,
response rates (as measured by decreased tumor volume and decreased
serum alpha-fetoprotein levels) were 60% to 83%.3,9-14 Cumulative
probability of survival ranged from 54% to 88% at 1 year, 33% to
64% at 2 years, and 18% to 51% at 3 years, with the best results
obtained by repeated embolizations with a combination of iodized
oil, Gelfoam (Upjohn, Kalamazoo, MI), and chemotherapeutic drugs.
Survival varies directly with oil uptake and retention, and
inversely with tumor volume, stage, and Childs class (figure
Despite the extent of single-institution experience with
chemoembolization of hepatoma published over the past decade, few
controlled trials have been reported. A multicenter European trial
lipiodol/Gelfoam chemoembolization to no therapy in 100 patients
with relatively small tumor burdens (90% stage I) found 1-year
survivals of 62% and 43% respectively, and 2-year survivals of 38%
and 26%.15 A French multicenter trial of 127 patients with more
advanced disease (62% stage II or III) showed almost identical
survival rates in the chemoembolization arm (64% and 38% at 1 and 2
years), with survival in the control arm of only 18% and 6%,
respectively (p <0.0001).16
Colorectal metastases-Phase II studies of chemoembolization for
metastatic colorectal cancer have been reported by several centers
in the United States. Patients enrolled in these trials are usually
individuals who have failed systemic and/or intra-arterial infusion
chemotherapy. Lang17 used a combination of superselective segmental
and selective lobar injections of a doxorubicin-iodized oil
emulsion on 46 patients; 59% achieved stabilization or regression
of disease with 17% complete responses. Actuarial survival was 68%
at 1 year and 37% at 2 years.
At the Boston Center for Liver Cancer, 40 patients were
chemoembolized with 5-FU, mitomycin-C, oil, and gelatin sponge.18
Sixty-three percent had partial or minor morphologic responses and
62% had a > 50% drop in CEA level. Median survival from first
chemoembolization was 10 months. A number of prognostic factors
were identified. Patients with an ECOG performance status of 0 to 1
had a median survival of 24 months, versus 3 months for those with
a performance status of 2. Patients with extrahepatic disease had a
median survival of 3 months versus 14 months for those without.
Among patients with good performance status and no extrahepatic
disease, actuarial survival was 73% at 1 year and 61% at 2 years.
Elevation of the alkaline phosphatase or LDH levels to above
3-times normal, or elevation of the AST above normal, all predicted
At Northwestern Memorial Hospital, 30 patients were
chemoembolized with cisplatin, doxorubicin, mitomycin-C (CAM), and
bovine collagen.19 They reported 95% of patients had a 3 25% drop
in CEA; 63% had a "radiologic" response, which was defined as tumor
necrosis or 3 25% decrease in size. Median survival was 8.6 months
from first chemoembolization and 29 months from diagnosis.
At the University of Pennsylvania, 51 patients were
chemoembolized with CAM, iodized oil, and PVA.20 Morphologic
stabilization or regression occurred in 72% of patients; CEA
stabilized or regressed in 90%; median duration of response was 12
months (figure 4). Actuarial survival from diagnosis with liver
metastases was 86% at 1 year, 55% at 2 years, and 23% at 3 years,
with a median survival of 24 months.
The results in these extensively pretreated patients are
promising, but high early response rates do not necessarily lead to
improved survival. Phase III trials of chemoembolization are needed
to determine if a survival benefit exists. The American College of
Radiology Imaging Network (ACRIN) is currently funding a
multicenter randomized trial of systemic chemotherapy with or
without chemoembolization for colorectal metastases to liver.
Ocular melanoma-Patients with ocular melanoma frequently develop
rapidly progressive, fatal hepatic metastases, with median
survivals of 2 to 6 months. The MD Anderson Cancer Center reported
results of 30 patients treated by serial chemoembolizations with
cisplatin and PVA.21 There was one complete response; 46% of
patients had a >50% morphologic response (figure 5). Median
survival was 11 months (14 months for responders versus 6 months
for non-responders), with an actuarial survival of about 33% at 1
year. There are no other large series for this tumor. Vogelzang22
reported dismal results using cisplatinum, doxorubicin,
mitomycin-C, and bovine collagen with only one long-term survivor
among eight patients, and a median survival of 2 to 3 months.
Neuroendocrine tumors-Embolization has an established role in
the palliation of these hypervascular tumors, typically producing
symptom-free intervals of 5 to 10 months in
> 90% of patients. Three reports have looked at
chemoembolization of neuroendocrine tumors23-25 (figure 6).
Response rates and survival are similar for embolization and
chemoembolization, but the duration of response after
chemoembolization averages close to 2 years. Other investigators
have warned of an increased complication rate after
chemoembolization of carcinoid tumors. A prospective randomized
trial is necessary to determine if there is enough additive benefit
from chemoembolization to justify any additional risk and cost.
Sarcomas-Mavligit26 reported major regression of metastatic
leiomyosarcoma in 10 of 14 patients with cisplatinum/gelfoam
chemoembolization, followed by a 2-hour vinblastine infusion into
the hepatic artery, with a median duration of response of 1 year.
Ten of 16 patients treated with CAM/oil/PVA at the University of
Pennsylvania responded, with extensive tumor necrosis demonstrated
on CT in all cases.27 Three became resectable. Median duration of
response was 10 months. Since systemic chemotherapy and
radiotherapy are ineffective against metastatic sarcomas in the
liver, chemoembolization is worthy of investigation.
Other metastases-Liver metastases from lung, breast, pancreas,
stomach, small bowel, kidney, bladder, thymus, cholangiocarcinoma,
ovary, thyroid, and unknown primary tumors have been treated with
chemoembolization. Published reports group patients with different
tumor types together, making interpretation of the results
difficult. Overall, mixed metastatic lesions have a 60% to 75%
objective response rate and median survivals of 8 to 11 months.
Percutaneous tumor ablation
A variety of chemical and physical agents have been used to
destroy cancerous tissue in the liver directly.28 Chemical
ablation, typically performed with absolute alcohol or acetic acid,
depends upon direct contact between the liquid sclerosant and the
tumor cells. Cell death occurs due to dehydration, protein
denaturation, coagulative necrosis, and small vessel thrombosis.
Areas of septation, necrosis, or other tissue inhomogeneity cause
incomplete diffusion of liquid agents through the tumor, which
limits the effectiveness of this technique. Complete necrosis is
achieved in 70% to 75% of small hepatomas, where the surrounding
cirrhotic liver helps to contain the alcohol within the tumor.
Alcohol is relatively ineffective for metastatic lesions, which
tend to be harder than the surrounding normal liver. Metastatic
disease is better treated using thermal ablation techniques, such
as cryotherapy or heating with radiofrequency, microwave, laser, or
focused ultrasound energy. These energized sources cause thermal
death within a predictable volume of tissue around the source
probe, irrespective of the nature of the tissue. The major
limitation of this technique is the heat sink caused by the
substantial blood flow within the liver, which limits the size of a
single thermal lesion to 2 to 3 cm with most devices.
Patient selection for
Similar to regional catheter-directed therapy, patients
undergoing percutaneous tumor ablation should have unresectable
disease confined to the liver. In addition, the tumor must be
visible and accessible to needle puncture under cross-sectional
imaging guidance (ultrasound, CT, or MR). Practical limitations
exist on the size and number of lesions that are likely to benefit
from this form of therapy. For tumors larger than 3 cm, multiple
overlapping chemical injections or thermal lesions must be
performed to completely treat the tumor volume and a 5- to 10-mm
margin of liver around the tumor. This becomes impractical once
tumors are larger than 5 cm, though some physicians aggressively
retreat such larger lesions in an effort to eliminate any residual
viable tumor. Treatment of more than 3 to 4 individual lesions not
only has practical limitations, but such patients are likely to
harbor additional sites of disease and, therefore, tend to progress
Technique of chemical ablation
Intravenous access is obtained for administration of analgesics.
The tumor is localized in the usual fashion as for a biopsy, and
the skin and liver capsule anesthetized. Specialized 20- to
22-gauge needles for alcohol ablation have a closed diamond tip and
multiple sideholes to facilitate distribution of the alcohol
through the tumor. Under imaging guidance, the needle is placed to
the far wall of the tumor, then alcohol is injected and the needle
gradually withdrawn toward the proximal margin. Ultrasound guidance
is preferable since it permits realtime observation of the
diffusion of the alcohol through the tumor. If the alcohol is
observed to track into vessels, bile ducts, the surrounding liver,
or back along the access tract, injection is halted and the needle
repositioned. Alcohol is also quite conspicuous on CT because of
its low density (-200 HU), but the injections cannot be monitored
in realtime. Once the injection is complete, the needle is left in
place for 1 to 2 minutes to allow the liquid to diffuse, then the
needle is withdrawn while aspirating, to avoid reflux of any
residual alcohol into the peritoneum. Additional passes may be
required to treat the entire tumor. The volume of alcohol required
is estimated using the formula for the volume of a sphere, adding
0.5 cm to the tumor radius to allow for ablation of a margin of
liver. Lesions up to 3 cm in diameter can be treated in a single
session. A 4-cm tumor requires 65 mL of alcohol, which is an
intoxicating and potentially toxic dose. Therefore tumors larger
than 3 cm, or multiple tumors, need to be treated in multiple
Pain, nausea, and vasovagal reactions are common during
percutaneous alcohol injection. Fever and elevation of liver
function tests occur during the ensuing few days. Complications
such as bleeding, pneumothorax, pleural effusion, liver abscess,
biliary stricture, hepatic infarct, and tumor seeding occur with a
frequency of <1% each.
Results of chemical ablation
Histologic examinations of resected hepatocellular carcinoma
nodules after alcohol ablation indicate complete tumor necrosis in
70% to 75% of tumors. For the usual patient not undergoing
resection, follow-up imaging is performed using triple-phase
scanning to examine the tumor during the arterial phase of contrast
enhancement. The overall size of the lesion after successful
ablation is larger due to ablation of a margin of normal liver, so
static imaging alone is not sufficient to assess response.
Peripheral rim enhancement is typical, and reflects the
inflammatory reaction in the surrounding liver. Any intratumoral
enhancement suggests residual viable tumor, which may be treated
with repeat ablation. Local recurrence rates at the ablation site
are 2% to 17%.29,30 As expected, almost all patients develop new
sites of disease elsewhere in the liver within 5 years, so
continuous surveillance is critical.
Survival after alcohol ablation of hepatocellular carcinoma is
reported to be 80% to 98% at 1 year and 55% to 70% at 3 years.
This, in part, reflects the early stage of disease in patients who
are candidates for local ablation, in contrast to patients treated
with chemoembolization, who have heavier tumor burdens at the time
Results of attempted alcohol ablation of metastatic liver
lesions are dismal, and this approach has largely been abandoned in
favor of thermal ablation.
Technique of thermal ablation
Currently, there are three commercially available radiofrequency
(RF) ablation devices in the United States for treatment of soft
tissue (figure 7). Each uses 15- to 18-gauge needles with either
multiple parallel needles or a radial array to disperse the energy
over a larger volume. The needle is placed into the lesion under
imaging guidance. Both CT and ultrasound work well for this
technique (figure 8). The exact protocol for needle placement and
delivery of the RF current varies by vendor. The endpoint for
treatment also depends upon the device, with varying use of time,
temperature, or electrical impedance as endpoints. This technology
is still relatively unstable, in that the vendors regularly
introduce more powerful generators and new probe configurations in
an effort to increase the treatment volume.
Using current technology, 3- to 4-cm tumors can usually be
ablated using overlapping burns (figure 9). Ablation of lesions
>5 cm is impractical, because it is difficult to achieve
complete treatment of the target volume, and local failure rates
are high. Time is also an issue since, depending upon the device
used, each burn requires 12 to 40 minutes.
RF ablation is extremely painful, and requires high levels of
analgesia and sedation. Other than pain, side effects are minimal.
Complications are similar to chemical ablation, but occur somewhat
more frequently due to the larger needle size and longer dwell time
in the liver. Careful placement of the grounding pads is important
to avoid thermal injury to the skin.
Results of thermal ablation
Immediate results of RF ablation based on follow-up imaging
indicate absence of any enhancing tumor in 60% to 90% of tumors,
with lesion size being the major determinant of success (figure
10). Local recurrence rates have been reported to be as low as 2%
to as high as 40% within 1 year.31 As with any local approach, new
lesions are the predominant mode of failure, occurring in up to 65%
of patients within 1 year. Comparison studies of RF ablation and
alcohol ablation for hepatocellular carcinoma demonstrate complete
ablation with fewer treatment sessions with RF ablation, and a
lower local recurrence rate.32 These advantages are believed to
offset the increased treatment time per session, the slight
increase in complications, and the increased cost for the device,
making RF ablation now the preferred treatment modality.
Combined regional and
Chemoembolization, while treating a large volume, is limited in
its ability to induce complete tumor necrosis. Conversely, RF
ablation causes thorough tissue necrosis within a small volume,
primarily limited by blood flow. Hence, combining the two
techniques is an appealing approach to intermediate size lesions.
Occlusion of the hepatic artery and/or portal vein during RF
ablation results in substantially larger burn volumes. This is
routinely done during intraoperative ablation using the Pringle
maneuver to temporarily reduce hepatic blood flow.
Chemoembolization, by devascularizing the tumor, allows effective
RF ablation of tumors up to 8 cm in diameter (unpublished data, May
2000). Blood flow to the surrounding liver is still preserved via
the portal vein, so a "surgical" margin is not achieved. Experience
with this combined modality therapy is still preliminary, so
long-term follow up for recurrence is not available, but the
immediate response is promising. AR
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