Biomed Imaging Interv J 2006; 2(3):e40
© 2006 Biomedical Imaging and
Radionuclide therapy of hepatocellular carcinoma
FX Sundram, MSc, DMRT
Nuclear Medicine and PET/CT Centre, Subang Jaya Medical Centre, Subang Jaya, Selangor, Malaysia
Hepatocellular carcinoma (HCC) is a malignant tumour of the
hepatocyte. It is a common malignancy worldwide and causes almost half a
million deaths annually. Asia is a high risk area. Although surgery
(hepatectomy or liver transplantation) is the main form of curative treatment,
the majority of patients are not eligible for surgery due to extent of tumour
and dysfunction of liver. Radiopharmaceuticals used for transarterial treatment
of HCC were Yttrium-90 microspheres, Iodine-131 lipiodol, Rhenium-188 lipiodol,
and Holmium-166 Chitosan complex. Yittrium-90 microspheres are glass or resin
microspheres of mean sphere diameter of 20 to 30 micrometre. The activity
administered was about 4 GBq. Reported response rate was about 20%, and median
survival was 54 weeks. On inoperable tumours, reported objective response of
I-131 lipiodol was 40 to 70%, and median survival was six to nine months. It
showed efficacy similar to TACE. In adjuvant treatment following curative
resection of HCC, reported three year survival was 86% compared with 46% for
the control group. The administered activity in both adjuvant and inoperable
HCC was about 2 GBq (55 mCi). Rhenium-188 lipiodol is a new radioconjugate, and
using it we treated 70 patients with inoperable HCC. This treatment was a part
of a multi-centre trial sponsored by the International Atomic Energy Agency.
Partial response was obtained in 17% of cases, while 49% had stable disease at
three months, and 34% showed disease progression. In terms of survival, 19% survived
one year, 60% for six months, and 90% for three months. The mean activity was
about 4.6 GBq (124 mCi). This method was safe and free from adverse effects. �
2006 Biomedical Imaging and Intervention Journal. All rights reserved.
Keywords: Hepatocellular carcinoma, iodine-131, lipiodol,
rhenium-188, yttrium-90 microspheres
Hepatocellular carcinoma (HCC) is a common malignancy
worldwide. It is a major cause of death from cancer in East Asia, especially China,
Japan, Korea, Taiwan, and Singapore. Sub-Saharan Africa, particularly Zimbabwe,
Ethiopia, and Mozambique faces a similar problem .
Surgical resection is generally accepted as the first choice
treatment for HCC. Only about 20% of all patients, however, have resectable HCC
at initial presentation, due to its multi-focal nature and frequent association
with cirrhosis . Treatment of inoperable HCC is mainly palliative. Many
non-surgical treatment modalities have been developed and used for the
treatment of HCC. These include percutaneous ethanol injection (PEI),
cryotherapy, radiofrequency ablation (RFA), systemic chemotherapy,
transarterial chemoembolisation (TACE), hormonal therapy, immunotherapy,
external radiotherapy, and radionuclide therapy.
PEI and RFA techniques have shown some success in the
treatment of small HCCs [4-6]. The use of cryotherapy, systemic chemotherapy,
hormonal therapy, immunotherapy, and external beam radiotherapy for the
treatment of HCC are either ineffective or have met with limited success [7-9].
Hepatic arterial blood flow can be obstructed by the injection of gelfoam or by
placing metallic coils. Flow obstruction can be combined with injection of a
mixture of lipiodol and chemotherapy drugs, also known as TACE. TACE is widely
used for the treatment of HCC , with the caveat that results are better in
well-selected patients . A randomised study by Raoul and co-workers has
shown a markedly better tolerance for I-131 lipiodol than for TACE with equal
long term outcome . Radionuclide therapy has been utilised for palliative
treatment of inoperable HCC and for adjuvant therapy following curative
resection of HCC.
Palliative Radionuclide Therapy for Inoperable HCC
The radionuclide is usually delivered via the hepatic
intra-arterial approach. Iodine-131 (I-131) lipiodol, Yttrium-90 (Y-90)
microspheres, and Rhenium-188 (Re-188) lipiodol are some of the
radiopharmaceuticals that have been utilised. Monoclonal antibodies, such as,
anticarcinoembryonic antigen and antiferritin labelled with Y-90 and I-131 have
also been utilised and are usually given parenterally. Other approaches, such
as, ultrasound-guided percutaneous intra-tumoral injection of Y-90 microspheres
have been used. Tian et al  treated 27 patients with HCC and six patients
with liver metastases using this approach, and they found encouraging results.
In their study, most of the patients failed other treatment modalities.
Twenty-seven patients were still alive 12 to 32 months after treatment, with
90.6% of the tumour foci becoming smaller. The serum α-fetoprotein (AFP)
levels were normalised in 10 out of 13 patients. Doses in the range of 282 Gy
to 757 Gy were delivered to the tumours.
I-131 emits both β and γ rays. The average energy
of the β rays emitted by I-131 is 181 keV and that of γ rays is 364
keV. It is, therefore, suitable for both therapeutic and imaging purposes. The
physical half-life of I-131 is 8.05 days. Lipiodol is an iodised ethyl ester of
the fatty acids of poppy seed oil containing 38% of iodine by weight. It is
known to selectively localise in HCC following intra-arterial hepatic
Many studies have reported encouraging results with the use
of I-131 lipiodol for the treatment of unresectable HCC [14-17]. The activity
of I-131 lipiodol administered ranges from 740 MBq to 6,220 MBq, either in
single or multiple treatments. Where the hepatic tumours were large,
fractionated doses of I-131 lipiodol were given at four-day intervals .
Repeat treatment can be given at intervals of 8 to 12 weeks. The objective
response rates, in terms of radiological regression of tumour and/or reduction
in serum α-fetoprotein levels, range from 40% to 70% [12,14]. Overall, the
response of HCC to intra-arterial I-131 lipiodol appears to be dependent on the
size of the tumour and the magnitude of the treatment dose delivered
transarterially. The response was poorer with increasing size of tumour and
lower administered treatment dose. This is to be expected from basic radiation
dosimetry principles, which relate cell death to radiation dose absorbed by a
The efficacy of hepatic intra-arterial I-131 lipiodol for
the treatment of HCC is comparable to TACE. I-131 lipiodol appears to be better
tolerated than TACE, with fewer side effects experienced by the patients.
Radionuclide therapy is, therefore, a reasonable alternative to TACE for the
treatment of unresectable HCCs. Two studies have compared the efficacy of
hepatic intra-arterial I-131 lipiodol therapy with TACE. In the study by
Bhattacharya et al, 69 patients with unresectable HCC received hepatic
intra-arterial epirubicin-lipiodol emulsion and 26 patients received hepatic
intra-arterial I-131 lipiodol . The survival benefit at 6 and 12 months for
either modality was comparable. The actuarial survival at 6, 12, and 24 months
was 40%, 25%, and 6%, respectively, with epirubicin-lipiodol, and 58%, 25%, and
0%, respectively, with I-131 lipiodol. Both groups showed acceptable toxicity,
such as, mild nausea, fever, and abdominal pain. In a French prospective randomised
trial , 142 patients were randomised to receive either intra-arterial
injection of I-131 lipiodol (73 patients) or chemoembolisation (69 patients).
It was found that in terms of patient survival and tumour response, both
modalities showed similar efficacy in the treatment of HCC. The overall
survival rates at six months, one, two, three, and four years were 69%, 38%,
22%, 14%, and 10%, respectively, in the I-131 lipiodol group and 66%, 42%, 22%,
3%, and 0%, respectively, in the chemo-embolisation group. Tolerance of I-131
lipiodol was significantly better with three severe side effects noted in the
I-131 lipiodol group and 29 in the chemoembolisation group (p <0.001).
There is also a role for I-131 lipiodol therapy in some
patients with portal vein thrombosis where TACE is generally contraindicated.
I-131 lipiodol does not modify arterial flow and appears feasible in some
patients with portal vein thrombosis. In a French randomised study , 14 HCC
patients were randomised to I-131 lipiodol therapy and 11 HCC patients to
medical support consisting of tamoxifen (five patients), intravenous 5
fluorouracil (one patient), and non-steroidal anti-inflammatory drugs or
corticosteroids (five patients). The survival rates at three, six, and nine
months were 71%, 48%, and 7%, respectively, for the treatment group and 10%,
0%, and 0%, respectively, for the control group. Overall, the tolerance was
excellent in the treated group.
In general, intra-arterial I-131 lipiodol treatment of HCC
is well-tolerated . Some reported side effects for this treatment include
fever, mild abdominal pain, nausea, elevation of transaminases, and radiation
hepatitis . Most of the side-effects are, however, mild and tend to resolve
with minimal or no intervention. Pre-treatment with Lugol�s iodine will result
in adequate thyroid uptake blockage. There may be a possible role for the use
of both radionuclide therapy and TACE together for palliative treatment of HCCs
as there may be a synergistic effect. Data on this form of combination therapy
are, however, lacking and further studies are awaited.
Y-90 is a stronger pure β emitter than I-131. It emits
β rays with an average energy of 935 keV and has a half-life of 64 hours
and a maximum penetration or β range of 11 mm. Y-90 does not emit γ
rays and is not optimal for imaging purposes. Y-90 can be embedded in
insoluble, non-biodegradable glass or resin microspheres (mean diameters of 25
�m to 35 �m). Administration of the Y-90 microspheres via the intra-hepatic,
intra-arterial route will result in the deposition of the glass or resin
microspheres in the tumour terminal vasculature. HCCs have a relatively greater
arteriolar density compared with the normal liver and are predominantly
supplied by the hepatic artery rather than the portal venous system. This will
result in a three-fold or greater radiation dose in the tumour nodules relative
to the normal liver . Y-90 microspheres can deliver a higher radiation dose
to the liver tumour compared with I-131 lipiodol. Y-90 microspheres can be
safely administered via intra-arterial injection to patients with HCC and
underlying cirrhosis at a dose of 100 Gy to the liver . With this
technique, an initial angiography scout dose with Tc-99m macroaggregated
albumin or other similar agent is required to document the presence of
significant porto-systemic shunting in the presence of portal hypertension.
Y-90 microspheres are generally not given when the lung uptake is >15%,
which indicates significant porto-systemic shunting. Extrahepatic shunting is
the main limitation to this form of therapy.
This form of therapy appears to be safe. Andrews et al
conducted a phase I dose escalation study using intra-arterial Y-90
microspheres with estimated whole liver nominal absorbed doses ranging from 50
Gy to 150 Gy . They did not find any haematologic, hepatic, and pulmonary
toxicity during a mean follow-up period of up to 53 months. Reversible
gastritis and duodenitis were encountered in four patients. Other reported side
effects associated with this form of treatment included fever, elevation of
liver enzymes and bilirubin, and gastrointestinal toxicities, such as, ulcers,
ileus, and nausea. Most of the side effects did not require treatment and
resolved spontaneously. There was one reported case of death resulting from
radiation pneumonitis. This patient, however, had 39% pulmonary shunting, and
it is questionable whether the patient should have been eligible for treatment.
Several studies have reported the use of Y- 90 microspheres
for the treatment of HCC [21-22]. The activity of Y-90 microspheres
administered ranged from 1,554 MBq to 5,000 MBq for initial treatment with
cumulative activity of up to 13,000 MBq from repeated treatments [23,24]. Using
the intra-arterial approach of administering the Y-90 microspheres, it is
possible to deliver radiation doses of up to 748 Gy to the tumour at a single
treatment session and cumulative tumour radiation doses of up to 1,580 Gy .
An objective response rate of 80%, in terms of reduction of serum
α-fetoprotein levels, has been reported . Other authors have reported
an objective response rate of 20% in terms of radiological regression of tumour
. Median survival of 9.4 months to 54 weeks has been achieved with the use
of Y-90 microspheres [21-25]. Interestingly, Lau et al reported four patients
whose tumours were converted into resectable ones and these underwent resection
. The disadvantage of this treatment is the high cost and the need for two
Re-188 has recently been used to treat HCCs. It has a
physical half-life of 16.9 hours and emits β rays with an average energy
of 795 KeV and γ rays of 155 KeV in 15% abundance. Gamma camera imaging
for biodistribution studies is possible with this radionuclide. Re-188 was
eluted from a W-188/Re-188 generator that has a long and a useful shelf life of
several months and, therefore, provides a constant yield of carrier-free Re-188
on a routine basis. This could potentially be cost-saving when compared to the
use of other radionuclides and would be particularly useful in the context of treating
HCC in developing countries, where incidence is among the highest in the world.
The concentrated elute from the tungsten-rhenium generator was heated with
4-hexadecyl 1-2, 9, 9-tetramethyl-4, 7-diaza-1, 10-decanethiol (HDD) in a water
bath for one hour to produce a rhenium-HDD complex. The HDD lyophilised kits
were obtained from Seoul National University Hospital in Korea. Lipiodol was
added and centrifuged to extract the Re-HDD into the lipiodol. This method of
preparation was previously described by Jeong et al  and Lee et al . An
International Atomic Energy Agency-sponsored multi-centre pilot study using
intra-arterial Re-188 lipiodol for the treatment of inoperable HCC showed
safety and efficacy of this radioconjugate . Sixteen patients were treated
with Re-188 lipiodol in this study. A �scout dose� was given, from which the
maximal tolerated dose (MTD) was determined using a specially designed
spreadsheet. The MTD is defined as the amount of radioactivity calculated to
deliver no more than 12 Gy to the lungs, 30 Gy to the liver, or 1.5 Gy to the
bone marrow. These doses have been found to be safe. This method of treatment
appears to be safe and well-tolerated at doses up to 7,400 MBq Re-188 lipiodol.
The side effects were minimal and included slight elevation of liver enzymes
(alanine transaminase and aspartate transaminase) at 24 hours, mild nausea,
mild hypochondrial pain, fever, and vomiting. The efficacy of this new
radionuclide for the treatment of HCC was confirmed in a larger, multi-centre
phase 2 study . Similar results were also reported by Lambert et al .
Table 1 below gives a summary of the various radionuclides used in the
treatment of HCC. Figure 1 shows a CT scan and Re-188 treatment scan. Figure 2
shows CT scans of liver tumour; Figure 3 shows the angiogram image; and Figure
4 shows the Yttrium-90 treatment dose image using the bremsstrahlung
Figure 1 CT scan and Rhenium-188 Lipiodol
treatment scan in a patient with HCC.
Figure 2 CT scan slices
of multifocal liver tumour.
Figure 3 Angiogram image
of multifocal tumour.
Figure 4 Bremsstrahlung
radiation image of Yttrium-90 treatment dose.
Table 1 A summary of the various radionuclides
used in the treatment of HCC.
Radio-labelled Monoclonal Antibodies to Treat HCC
There are a few monoclonal antibodies against antigens, such
as, CEA, ferritin, and α-fetoprotein, which have some degree of
specificity for HCC. Both anti-CEA and antiferritin antibodies have been
labelled with I-131 and Y-90 and are administered parenterally for the
treatment of HCC. The results have been encouraging, although experience with
this method of treatment is limited to only a few centres. The efficacy of this
form of treatment may be limited by the fact that the tumour cells are
generally heterogeneous and not all the cells express the same antigen. There
is also a possibility of developing human-antimouse antibodies with the use of
antibodies of murine origin. This will prevent subsequent treatment.
Adjuvant Treatment with I-131 Lipiodol after Curative
Resection of HCC
Resection of HCC is potentially curative, but the recurrence
rate is 100% at 5 years. It is hypothesised that the high recurrence rate is
due to microscopic metastatic disease or metachronous multicentric tumour
present in the remnant liver not detected before and at the time of surgery by
the usual imaging methods. Various systemic and locoregional chemotherapy
agents have been tried to reduce the rate of recurrence. The overall results
show marginal or no significant improvement in disease-free survival. The
efficacy of these forms of therapy is also limited by the toxicity of the
chemotherapeutic agents. The presence of underlying cirrhosis further limits
the ability of the liver remnant to tolerate these agents. In adjuvant therapy,
there appears to be a role for radionuclide therapy in improving disease-free
and overall survival following curative resection of HCC. Lau et al randomised
21 patients to receive one 1,850 MBq dose of intra-arterial I-131 lipiodol and
22 patients to no adjuvant treatment following curative resection of HCC .
The median disease-free survival in the treatment and control groups was 57.2
months and 13.6 months, respectively. The three-year overall survival for the
treatment and control groups was 86.4% and 46.3%, respectively. In a more
recent study, Partensky et al reported a median time to detected recurrence of
28 months (range 12 to 62 months) for 28 patients . Each patient was
treated with one 1,110 MBq dose of intra-arterial I-131 lipiodol following
curative resection of HCC. The overall survival rates were 86% at three years
and 65% at five years. In our preliminary study, the six-month disease-free
survival rate was 100% and the 12-month disease-free and overall survival rates
were 72% and 85%, respectively, for 15 patients who had received I-131 lipiodol
adjuvant therapy following curative resection of HCC . This form of
adjuvant therapy appears to be safe with no clinically adverse side effects
reported. Adjuvant radionuclide therapy may also have a possible role in
reducing the rate of tumour recurrence after minimally invasive percutaneous
treatment of small HCC, such as, PEI and RFA.
Some work has been done using P-32 glass micospheres
intrarterially, and the results are similar to TACE alone . Re-186 and Re-188
glass microspheres have been effective in animal models, but clinical data are
lacking . Ho-166 microspheres and chitosan complex are used in Korea for
the treatment of inoperable HCC .
Treatment of HCC involves multi-disciplinary collaboration.
In cases of multi-segmental or large HCCs, palliative treatment using
radionuclide therapy is a viable alternative to TACE. The survival rates are
similar for both modalities, but radionuclide therapy appears to be better
tolerated with less severe side effects. In rare instances, unresectable
tumours may be converted to respectable tumours after radionuclide therapy.
Radionuclide treatment in a curative intent may be possible for small HCCs in
instances where surgery or percutaneous treatment is not possible due to tumour
location or severe concurrent medical illnesses. Adjuvant radionuclide therapy
appears to have a promising role in reducing the rate of tumour recurrence
after surgery for resectable HCCs and after percutaneous treatment of small
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| Received 19 May 2006; received in revised form 30 June 2006, accepted 24 July 2006
Correspondence: Subang Jaya Medical Centre, 1 Jalan
SS 12/1A, 47500 Subang Jaya, Selangor, Malaysia. Tel.: +603-
56306383; Fax.: +603- 56335910; E-mail: firstname.lastname@example.org
Please cite as: Sundram FX,
Radionuclide therapy of hepatocellular carcinoma, Biomed Imaging Interv J 2006; 2(3):e40
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