Long-term Results of Percutaneous Ethanol Injection for the Treatment of Hepatocellular Carcinoma in Korea

Abstract

To evaluate the long-term follow-up results of percutaneous ethanol injection (PEI) for the treatment of hepatocellular carcinoma (HCC) in Korea.
Sixty-eight nodular HCCs initially detected in 64 patients, were subjected to US-guided PEI as a first-line treatment. Long-term survival rates, local tumor progression rates, and complications were evaluated, as were the influences of tumor size and Child-Pugh class on these variables.
No major complications occurred. The overall survival rates of the 64 patients at three and five years were 71% and 39%, and their cancer-free survival rates were 22% and 15%, respectively. The overall survival rate of patients with a small HCC (< or =2 cm) was significantly higher (p = 0.014) than that of patients with a medium-sized HCC (< or =2 cm). The overall survival rate of patients with Child-Pugh class A was significantly higher (p = 0.049) than that of patients with Child-Pugh class B. Of 59 cases with no residual tumor, local tumor progression was observed in ablation zones in 18, and this was not found to be significantly influenced by tumor size or Child-Pugh class.
The results of our investigation of the long-term survival rates of PEI in HCC patients in Korea (a hepatitis B virus-endemic area) were consistent with those reported previously in hepatitis C endemic areas. Patients with a smaller tumor or a better liver function exhibited superior survival rates.

Full text

Korean J Radiol 7(3), September 2006 187
Long-term Results of Percutaneous
Ethanol Injection for the Treatment of
Hepatocellular Carcinoma in Korea
Objective: To evaluate the long-term follow-up results of percutaneous ethanol
injection (PEI) for the treatment of hepatocellular carcinoma (HCC) in Korea.
Materials and Methods: Sixty-eight nodular HCCs initially detected in 64
patients, were subjected to US-guided PEI as a first-line treatment. Long-term
survival rates, local tumor progression rates, and complications were evaluated,
as were the influences of tumor size and Child-Pugh class on these variables.
Results: No major complications occurred. The overall survival rates of the 64
patients at three and five years were 71% and 39%, and their cancer-free survival
rates were 22% and 15%, respectively. The overall survival rate of patients with a
small HCC ( 2 cm) was significantly higher (p = 0.014) than that of patients with
a medium-sized HCC ( 2 cm). The overall survival rate of patients with Child-
Pugh class A was significantly higher (p = 0.049) than that of patients with Child-
Pugh class B. Of 59 cases with no residual tumor, local tumor progression was
observed in ablation zones in 18, and this was not found to be significantly influ-
enced by tumor size or Child-Pugh class.
Conclusion: The results of our investigation of the long-term survival rates of
PEI in HCC patients in Korea (a hepatitis B virus-endemic area) were consistent
with those reported previously in hepatitis C endemic areas. Patients with a
smaller tumor or a better liver function exhibited superior survival rates.
ercutaneous ethanol injection (PEI) is a low-risk, well-established
treatment for patients suffering from cirrhosis and a relatively early-stage
hepatocellular carcinoma (HCC). Since early reports regarding the
therapeutic efficacy of PEI were issued (1 4) and subsequent reports on medium-term
survival results (5 9), the long-term therapeutic efficacy of PEI for HCC has been
addressed by several investigators (10 14). The majority of these studies have been
conducted in Japan, Italy, and Spain; all hepatitis C endemic areas. However,
relatively few reports have addressed long-term (5 years or longer) survival in hepati-
tis B endemic areas, which include China, Taiwan, Vietnam, Korea, and certain
African countries. A Korean report and two Taiwanese papers, which included
medium-term (3-year) survival results, found one, two, and three year overall survival
rates for PEI of 85 98%, 61 96%, and 50 88%, respectively (15 17). Thus, the
objective of the present study was to characterize the long-term results of PEI for HCC
in Korea, a hepatitis B endemic area.
MATERIALS AND METHODS
Between January 1995 and April 1999, 64 patients with 68 nodular HCCs were
Yon Mi Sung, MD1,2
Dongil Choi, MD1
Hyo K. Lim, MD1
Won Jae Lee, MD1
Seung Hoon Kim, MD1
Min Ju Kim, MD1
Seung Woon Paik, MD3
Byung Chul Yoo, MD3
Kwang Cheol Koh, MD3
Joon Hyoek Lee, MD3
Moon Seok Choi, MD3
Index terms:
Liver, neoplasms
Liver neoplasms, therapy
Alcohol ablation
Korean J Radiol 2006;7:187-192
Received October 31, 2005; accepted
after revision February 7, 2006.
1Department of Radiology and Center for
Imaging Science, Samsung Medical
Center, Sungkyunkwan University School
of Medicine, Seoul 135-710; 2Department
of Radiology and Center for Imaging
Science, Eulji Medical Center, Eulji
University School of Medicine, Daejeon
302-799; 3Department of Medicine,
Samsung Medical Center, Sungkyunkwan
University School of Medicine, Seoul 135-
710, Korea
Address reprint requests to:
Dongil Choi, MD, Department of
Radiology and Center for Imaging
Science, Samsung Medical Center,
Sungkyunkwan University School of
Medicine, 50, Ilwon-dong, Kangnam-gu,
Seoul 135-710, Korea
Tel. (822) 3410-2518
Fax. (822) 3410-2559
e-mail: dichoi@smc.samsung.co.kr
P

treated by PEI as a first-line treatment at our institution.
The study subjects comprised 41 men and 23 women,
ranging from 34 to 87 years old (mean, 59 years). Fifty-six
patients tested positive for serum hepatitis B surface
antigen, and seven tested positive for anti-hepatitis C virus
antibody. Fifty-five patients exhibited cirrhosis following
hepatitis, eight had chronic active hepatitis, and one
patient showed no evidence of a liver pathology. At the
time of PEI treatment, the numbers of Child-Pugh class A
and B liver cirrhosis patients were 32 and 23, respectively.
All of the included patients fulfilled the following criteria
for PEI treatment: a single nodular HCC of < 4 cm in
maximum diameter; multinodular HCCs (up to three in
number), and each tumor < 3 cm in maximum diameter;
tumors were accessible via a percutaneous approach; the
absence of portal venous thrombosis or extrahepatic
metastases; Child-Pugh class A or B liver cirrhosis; a
prothrombin time ratio > 40%, and a platelet count >
40,000/mm3(40 cells 109/L). This study was approved by
our institutional review board, and written informed
consent was provided by all patients.
Hepatocellular carcinoma diagnoses were verified using
ultrasound (US)-guided percutaneous needle biopsies in 63
of the 68 masses (92.6%). The remaining 5 tumors were
considered to be HCCs based on characteristic imaging
findings and elevated levels of serum -fetoprotein (AFP).
Small HCCs and medium-sized HCCs were defined as
being 2 cm in diameter and > 2 cm in diameter, respec-
tively. HCCs were graded histologically as well differenti-
ated, moderately differentiated, or poorly differentiated in
accordance with the Liver Cancer Group of Japan’s classi-
fication of primary hepatic cancer.
All of patients underwent conventional, multisession US-
guided PEI (total session, 248; mean session per tumor,
3.65). The needle used for these procedures were 21-gauge
needles, with three side holes, and no end hole (PEIT
Needle; Hakko, Tokyo). The total amount of alcohol
injected was determined by tumor diameter: 8 ml for
lesions of 1.0 cm in diameter, 15 ml for 2.0 cm lesions, and
25 ml for 3.0 cm lesions. Injections were performed two or
three times a week, depending on patient tolerance, until
the total amount of alcohol injected reached the intended
volume. Three to eight milliliters of ethanol were adminis-
tered to each tumor until the ethanol distributed through-
out a tumor or until ethanol leakage from a tumor was
observed.
Immediate US was conducted in order to evaluate any
emergent complications, and therapeutic efficacy was
assessed from US, CT, and AFP assays, one month after
PEI treatment completion. Patient response was considered
complete when sequential CT scans evidenced no areas of
contrast material enhancement in a lesion, and when CT
and US scans indicated no increase tumor size. In cases
with evidence of technical success with no new lesions by
one month follow-up CT, subsequent follow-up CTs were
administered at 3-month intervals.
When, during follow-up, our imaging methods revealed
local recurrences or new lesions that were treatable,
additional PEI, percutaneous transarterial chemoemboliza-
tion, radiofrequency ablation, surgery, or combinations
thereof were conducted.
Follow-up times ranged from three to 99 months
(median, 50 months; mean, 43.6 months). Of the 64
subjects, 13 (20.3%) were followed-up for five years or
more.
Cumulative overall and cancer-free survival rates were
calculated using the Kaplan-Meier method. The log-rank
test was employed to determine differences in survival
rates with respect to; tumor size, histopathologic grades,
and Child-Pugh classification. Differences in local tumor
progression rates with respect to tumor size and Child-
Pugh classification were calculated using Chi-square and
Fisher’s exact tests. These calculations were carried out
using SPSS software (SPSS for Windows; SPSS Inc.,
Chicago, IL).
RESULTS
Tumor sizes in our study patients ranged between 0.8
and 4 cm (mean 2.1 cm); in 39 patients, 43 HCCs were
found that were 2 cm in diameter, and in 25 patients, 25
HCCs that were in > 2 cm in diameter. The degree of
histopathologic differentiation was assessed using
Edmonson grade, as follows; 18 tumors grade I, 23 tumors
grade II, 15 tumors grade III, three tumors grades I or II,
and four tumors of grades II or III.
At the end of this study, 20 patients remained alive, and
38 patients had succumbed. Six patients were lost to
follow-up. The cumulative overall and cancer-free survival
curves of the 64 study subjects are shown in Figure 1.
Overall survival rates at one, two, three, and five years
were 92%, 81%, 71%, and 39%, respectively, and the
corresponding cancer-free survival rates were 56%, 30%,
22%, and 15%, respectively.
One , 2 , 3 , and 5 year survival rates were 95%,
90%, 76%, and 55%, respectively, for the 39 patients
with tumors 2 cm in largest dimension; and were 88%,
67%, 63%, and 17%, respectively, for the 25 patients
with HCCs > 2 cm in largest dimension (Fig. 2). Mean
survival of patients with a HCC 2 cm in diameter was
significantly longer (p = 0.014) than that of patients with a
HCCs > 2 cm in diameter. The ages (p = 0.855), sexes (p =
Sung et al.
188 Korean J Radiol 7(3), September 2006

0.458), and Child-Pugh classes (p = 1.000) of patients a
HCC 2 cm or > 2 cm in diameter were not significantly
different.
Mean 1 , 2 , 3 , and 5-year survival rates were
estimated to be 91%, 80%, 75%, and 38%, respectively,
for the 21 patients with well-differentiated HCC (grade I
or I > II); and 91%, 78%, 65%, and 33%, respectively, for
the 38 patients with moderately- or poorly differentiated
HCCs (grade II, III or grade II > I), and no statistically
significant difference was found between these two differ-
entiation-based groups (p = 0.705).
For patients with Child-Pugh class A cirrhosis of the liver
(n = 32), the 1 , 3 , 5 , and 6-year survival rates were
100%, 84%, 48%, and 36%, respectively, and these
figures were significantly higher (p = 0.049) than those of
patients with Child-Pugh class B (n = 23), who had survival
rates of 82% at one year, 55% at three years, 21% at five
years, and 11% at 6 years (Fig. 3). The ages (p = 0.696)
and sexes (p= 0.254) of Child-Pugh class A and Child-
Pugh class B patients were not significantly different.
During follow-up examinations, of 59 tumors (in 59
patients) with no residual tumor, local tumor progression
in ablation zones was detected for 18 tumors (31%). The
local tumor progression rates were 23% (9 of 39 HCCs)
for tumors 2 cm in diameter, and 45% (9 of 20 HCCs)
for tumors > 2 cm. For 50 tumors in cirrhotic livers, local
tumor progression rates were 30% (9 of 30 HCCs) in
patients with Child-Pugh class A, and 20% (4 of 20 HCCs)
in patients with Child-Pugh class B, and no significant
relation was found between tumor size (p = 0.161) and
Child-Pugh class (p = 0.522).
No major complications occurred among a total of 248
PEI sessions, an average of 3.65 sessions per tumor.
Follow-up CT showed intraperitoneal hemorrhage in two
patients, but these resolved spontaneously.
DISCUSSION
Percutaneous ethanol injection has been widely
Percuteneous Ethanol Injection Therapy for Hepatocelluar Carcinoma
Korean J Radiol 7(3), September 2006 189
Fig. 1. The cumulative overall and cancer-free survival curves of
our 64 study subjects with hepatocellular carcinoma, who treated
by percutaneous ethanol injection.
Fig. 2. Cumulative survival curves of the 64 hepatocellular
carcinoma patients after percutaneous ethanol injection
treatment, according to tumor size. The survival rates of patients
with a hepatocellular carcinoma of 2 cm in diameter (n = 39,
black line) were determined to be significantly higher (p= 0.014,
log-rank test) than those of patients with as hepatocellular
carcinoma of 2 cm in diameter (n = 25, gray line).
Fig. 3. The cumulative survival curves of 55 hepatocellular
carcinoma patients after percutaneous ethanol injection
treatment, with respect to the Child-Pugh classification of the
clinical stage of coexistent cirrhosis of the liver. The survival rates
of class-A patients (n = 32, black line), and class-B patients (n =
23, gray line) were significantly different (p= 0.049, log-rank test).

employed to treat HCCs smaller than 3 to 5 cm (7, 9, 10,
12 14, 18). Because of its strong dehydrating effect,
ethanol induces the immediate coagulative necrosis of
tumor cells, and enables the complete ablation of small
neoplastic lesions, without adversely affecting liver
function (1, 3 6, 19 21).
Several studies on survival after PEI have been reported
in hepatitis C endemic areas, such as, Japan and Italy. As
compared with HCCs in patients with hepatitis C
infections, HCCs related to hepatitis B infections show
larger, more infiltrative, and a greater frequently of
multiple tumors at first imaging, and in addition,
recurrences are more commonly after treatment (15, 22,
23). However, the underlying hepatic functional reserves
in patients with hepatitis B associated HCC are usually
better than those with hepatitis C associated HCC (22).
According to one report, after surgical resection, patients
with hepatitis B associated HCC showed poorer survival
than patients with hepatitis C associated HCC (23).
In our study, we obtained 3-year and 5-year survival
rates of 71% and 39%, respectively. Survival reached
76% at three years and 55% at five years, in patients with
a tumor of 2 cm in diameter, and 63% at 3years, and
17% at 5 years, in patients with a tumor > 2 cm in
diameter. These results are consistent with those reported
by other investigators in areas in which the hepatitis C
virus is endemic (10 14). Moreover, these similar survival
figures demonstrate the reliability and reproducibility of
the PEI technique. In addition, several investigators have
shown that survival rates are influenced by tumor size and
Child-Pugh class (10, 11), and our findings concur.
In the present study, the survival rates of Child-Pugh
class A patients were 48% at five years and 36% at six
years. These figures are similar to those obtained for
patients treated by hepatic resection (10, 24). Surgical
resection in early-stage HCC was reported to result in 5-
year survival rates of 41 51% (25 27). Yamamoto et al.
(24) also examined the efficacies of PEI and surgical
resection for the treatment of small HCCs, and found that
3- and 5-year overall survival rates were almost identical
(82.1%, and 59.0%, respectively, in the PEI group;
84.4%, and 61.5%, respectively, in the surgical group).
Although no prospective, randomized trials have been
conducted to compare the efficacies of PEI and surgery,
their long-term results appear comparable.
Moreover, a comparison of relevant data demonstrated
that survival after PEI tends to be superior to survival after
conventional transarterial chemoembolization. The mean
5-year survival rate shown by 556 patients with HCC
lesions of < 5 cm, all of whom had been treated by conven-
tional transarterial chemoembolization, was only 14%
(10). However, transarterial chemoembolization may
cause liver functions to worsen, because the technique also
damages noncancerous liver parenchyma (28, 29).
However, more recent results obtained for segmental and
subsegmental transarterial chemoembolization have been
more encouraging (30 32).
Some recent reports have asserted that the local tumor
progression rate after PEI is about 33 43% (33, 34),
which is consistent with our findings (31%). However, this
high tumor recurrence rate does not represent a compara-
tive limitation of PEI, as similar rates are frequently found
in cirrhotic patients with HCC treated with any therapeutic
modality, including surgery (35, 36). Moreover, in the
present study, tumor size and Child-Pugh class were found
to be related to local tumor progression.
Radiofrequency ablation is now replacing PEI for the
treatment of HCCs, because of its higher rate of complete
necrosis, requirement for fewer treatment sessions, and
higher cancer-free survival rates (37 40). However, in
terms of cost, PEI is definitely superior to radiofrequency
ablation. In our experience, PEI should be recommended
particularly for diminutive HCCs (< 1.5 cm), including
residual and recurrent tumors, because treatment with
probably require only one or two PEI sessions.
However, our study has its limitations. First, a number of
the patients enrolled in this study were also treated using
modalities other than PEI. Multimodal treatments, includ-
ing repeat PEI, transarterial chemoembolization, radiofre-
quency ablation, and surgery were conducted in cases with
residual or recurrent tumors, i.e., PEI in four, transarterial
chemoembolization in 16, radiofrequency ablation in nine,
surgical resection in three, radiofrequency ablation and
transarterial chemoembolization in 11, PEI and transarter-
ial chemoembolization in six, and surgical resection and
radiofrequency ablation in two. This is also an inherent
limitation of similar prior studies. Second, the proportion
of censored data was relatively high. The retrospective
nature of this study made it difficult to perform adequate
follow-up examinations for all patients, and survival was
confirmed by telephone interview with a family member
for 23 of 64 patients, which made it impossible to
determine cumulative local or remote site tumor
recurrence rates. Third, the relation between survival rate
and tumor location was not assessed, because of the
retrospective nature of the study, it was difficult to assess if
HCCs were located in the periphery or the center of livers
using only transverse CT images.
In conclusion, our study demonstrates the long-term
effectiveness of PEI for the treatment of HCC in a hepatitis
B virus endemic area. Our long-term survival results for
HCC patients treated with PEI are comparable to those
Sung et al.
190 Korean J Radiol 7(3), September 2006

previously reported in hepatitis C endemic areas.
Unsurprisingly, both tumor size and degree of liver
function were found to significantly affect survival rates
and times. Although radiofrequency ablation is rapidly
replacing PEI as a treatment modality, PEI still appears to
be both effective and safe for the treatment of small HCCs.
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