INTRODUCTION
In the non-surgical treatment of hepatocellular carcinoma
(HCC), conventional trans-arterial chemoembolization (CTACE),
which uses lipiodol as a drug vehicle to deliver anticancer
agents, has been in use for over 40 years. In 2002, two
randomized controlled clinical trials confirmed its value in
standard palliative treatment of unresectable HCC,1,2 which
was subsequently confirmed by the publication of two metaanalyses.3,4 Drug-eluting beads trans-arterial chemoembolization
(DEB-TACE) has been widely implemented in the West, replacing
C-TACE, and has been recently implemented in Korea.
The background of the DEB-TACE concept can be seen
as a result of trying to improve the weaknesses of each of the
components of C-TACE. First, the complex emulsion of lipiodol
and anticancer agent used in C-TACE is not a true
chemical bond; therefore, the components are separated
within a short period of time, causing efflux of a large amount
of anticancer drug into the systemic vein, and resulting in
systemic side effects and deterioration of local anti-cancer effectiveness.
Second, lipiodol itself is a very fine capillary level
embolic droplet. In addition to inducing post-embolization
syndrome (PES) in most patients, a lipiodol-anticancer emulsion
stimulates micro-capillary damage to the peri-biliary
plexus, resulting in irreversible complications such as progressive
biliary injury, peri-biliary biloma, portal vein thrombosis,
liver infarction, liver abscess, and even mortality from
liver failure and sepsis.5 Third, in C-TACE, gelatin sponge
particles or poly-vinyl alcohol particles are used as an embolization
material to block the arterial blood flow. However, it is
difficult to perform compact distal embolization because its
shape is irregular and the size is not constant. The use of drug-eluting beads aims to improve the drugdelivery
system and the embolic material, which are the problems
of C-TACE, while maintaining the basic principles of
TACE. Theoretically, by controlling anti-cancer drug efflux
to the whole body through reversible ionic-exchange of the
cancer drug and the drug vehicle, and maximizing a constant
concentration of the anti-cancer drug delivered to the inside
of the HCC and periphery of tumor bed for a certain period, DEB-TACE could become accepted for the treatment of
HCC. Moreover, microspheres are a uniform shape and size
and show a better distal compact embolic effect with DEBTACE.6,7 However, microspheres as a drug carrier are a permanent
embolic material. Therefore, the question arises regarding
how many repeat procedures can be performed
considering local tumor recurrence and frequent occurrence
of HCC, especially in cases of very early small recurrence
within a tight regular imaging follow-up. Because drug-eluting
beads are larger than lipiodol, there is limited drug delivery
and embolization to the portal vein side. In addition,
since it uses a permanent embolic material, it can be difficult
to apply DEB-TACE in a repeat second session of treatment. It is clear that both C-TACE and DEB-TACE have their
own advantages, and disadvantages or problems, and there
are few large comparative papers on this subject, especially in
the treatment of very early and early stages of HCC. Therefore,
the purpose of this study is to compare these modalities
as an initial treatment for HCC in a very early or early stage.
METHODS
We retrospectively analyzed and compared the use of CTACE
and DEB-TACE for the treatment of HCC from September
2009 to May 2016 using a controlled-match method. Baseline characteristics of C-TACE and DEB-TACE groups
are summarized in Table 1. There was no difference between
the groups with regard to patient demographics, underlying
liver disease, tumor staging, liver function, tumor size, and
tumor markers. All patients were in a very early (stage 0) or early stage
(stage A) of the Barcelona Clinic Liver Cancer (BCLC) staging
system.8-10 All patients had Child–Pugh class A or ≤B7
liver status. The inclusion criteria were follows: clinically or histologically
diagnosed HCC according to the American Association
for the Study of Liver Disease (AASLD) criteria,11 no previous
therapy, single HCC, Child-Pugh class ≤B7, 1–5 cm maximum
diameter and segmental involvement. Exclusion criteria
were as follows: post-TACE follow-up period less than one
year, Eastern Cooperative Oncology Group (ECOG) perfor-mance status ≥ 1, infiltrative/pedunculated/cirrhotomimetic
morphology, bile duct invasion, vascular invasion, hepatofugal
portal flow, total bilirubin ≥ 3 mg/dL. Informed consent for TACE with both methods was obtained
from all patients. Approval by the institutional review
board was waived because the study was retrospective. Before TACE, diagnostic angiography of the superior mesenteric
artery and celiac trunk (or common hepatic artery)
was performed using a 5-Fr angiographic catheter under local
anesthesia via the common femoral artery approach to check
for portal vein patency and maintained hepatopetal portal
flow, to map hepatic arterial anatomy and to identify tumor
feeding arteries of the HCC. In cases of multiple tumor feeding
arteries, segmental arteries were selectively catheterized,
whereas in smaller lesions with subsegmental tumor feeding
artery, the subsegmental branch artery was superselected.
Feeding arteries were selectively or superselectively catheterized
using a microcatheter (2.0-Fr. Progreat® α, Terumo®, Tokyo, Japan) with an appropriate microguide wire (0.016-
inch Radiofocus® GT, Terumo®, Tokyo, Japan; 0.016-inch FathomTM, Heredia, Costa Rica). C-TACE (n=115) was performed
using a mixture of lipiodol and doxorubicin (Adriamycin
RDF; Ildong Pharmaceutical, Seoul, Korea), followed
by embolization of the feeding artery using gelatin sponge
particles. The maximum amount of lipiodol and doxorubicin
was 10 mL and 50 mg, respectively. For DEB-TACE, two types of DEB were used, DC beads (Biocompatibles, Farnham,
Surrey, UK; n=75), or Hepasphere (Biosphere Medical,
Roissy, France; n=28) loaded with a maximum amount of 75
mg of doxorubicin per vial to 150 mg of doxorubicin loaded
in two vials of DEB. For DC beads, in cases of small HCC
with minimal vascularity, 100–300 µm sized beads were chosen.
If the HCC was large and vascularity was rich, we selected
DC beads with a diameter of 300–500 µm or a combination
of both sizes of DC beads, i.e., 100–300 µm sized beads
first to embolize more distally, and then 300–500 µm sized
beads for proximal larger arteries. The hepasphere has a different
mechanical property, it is a dry form, but become
swollen in an aqueous condition, predictably by almost 4-fold
in contrast media. For instance, 50–100 µm hepasphere beads
in dry form can expand to 200–400 µm when hydrated in contrast media. A 50–100 µm sized dry form was used in this
study, resulting in 200–400 µm sized hydrated microspheres.
The end point of C-TACE was the opacification of peritumoral
portal veins by lipiodol and doxorubicin emulsion.
The end point of DEB-TACE was defined as complete stasis
of blood flow of the feeding artery for at least 10 seconds and
no residual tumor staining from the target artery. For comparison of the C-TACE and DEB-TACE methods,
the following parameters were evaluated: severe pain and bradycardia
during TACE, PES, changes in liver function, complications,
target tumor response assessed by the European Association for the Study of the Liver (EASL) criteria,12-15 and
conversion to another treatment modality. All patients were followed up with computed tomography
(CT) or magnetic resonance imaging (MRI) within 1 month
after TACE, and then at 3-month, 6-month and 1-year unless
residual tumor or local tumor recurrence was evident. Numeric differences between groups were assessed by the
independent Student’s t test for continuous variables and by
chi-square test for categorical variables. The statistical results
were considered to indicate significance if the P-value was less
than 0.05.
Table 1. Baseline characteristics of C-TACE and DEB-TACE groups (no
significant difference between groups)

C-TACE, conventional-trans-arterial chemoembolization; DEBTACE,
drug-eluting beads-trans-arterial chemoembolization; BCLC,
Barcelona clinic liver cancer; HCC, hepatocellular carcinoma; α
-FP, alpha-fetoprotein; PIVKA-II, prothrombin induced by vitamin K
absence or antagonist-II.
RESULTS
1. Severe pain and bradycardia during TACE
(Table 2)
The incidence of severe intractable pain during the TACE
procedure was significantly higher in the C-TACE group
(103/115 patients, 89.6%) than in the DEB-TACE group
(12/103, 11.6%) (P<0.001). Most cases in the superselective
C-TACE group required intravenous administration of the
maximum dose of pethidine HCl (50 mg) and fentanyl citrate
(100 µg). In cases of profound pain in the C-TACE group,
bradycardia was accompanied in 30.4% of patients (P<0.001);
in such cases, intravenous administration of atropine was
mandatory. In all cases, the bradycardia-induced hypotension recovered in a couple of minutes after intravenous administration
of atropine.
Table 2. Severe pain and bradycardia during the TACE procedure

TACE, trans-arterial chemoembolization; C-TACE, conventional-trans-arterial chemoembolization; DEB-TACE, drug-eluting beads-trans-arterial
chemoembolization.
*Intravenous administration of atropine was mandatory in cases of bradycardia.
2. PES (Table 3)
The incidence of PES was significantly higher in the CTACE
group than in the DEB-TACE group immediately after
the procedure (P<0.001). Once there was improvement of the
immediate PES symptoms and laboratory findings, the patient
was discharged, and the duration of PES was determined
at the 1-month out-patient visit. The duration of PES was
also significantly longer in the C-TACE group than in the
DEB-TACE group ( P<0.001). A longer duration of PES was
observed in cases with serious complications such as acute
ischemic cholecystitis, liver parenchymal infarction, liver abscess,
or biliary tree necrosis.
Table 3. Post-embolization syndrome (PES)

C-TACE, conventional-trans-arterial chemoembolization; DEB-TACE, drug-eluting beads-trans-arterial chemoembolization.
3. Changes in liver function (Table 4)
The immediate post-TACE increases in the liver enzymes
aspartate aminotransferase (AST) and alanine aminotransferase
(ALT) were significantly higher in the C-TACE group
than in the DEB-TACE group (P<0.001). In the C-TACE
group, the mean±SD elevation of liver enzymes (AST and
ALT) was 3.5±1.5-fold and 3.8±1.5-fold, respectively. In contrast,
for DEB-TACE, the mean±SD elevation (AST and
ALT) was 1.4±0.7-fold and 1.6±0.7-fold, respectively. Deterioration of Child-Pugh class during the follow-up period was
also significantly higher in the C-TACE group than in the
DEB-TACE group (P=0.006). In the C-TACE group, worsening
of Child-Pugh class occurred in 25.2% of patients, compared
with 10.7% for DEB-TACE.
Table 4. Change in liver function

AST, aspartate aminotransferase; ALT, alanine aminotransferase; C-TACE, conventional-trans-arterial chemoembolization; DEB-TACE, drug-eluting
beads-trans-arterial chemoembolization.
4. Serious complications (Table 5)
There was no significant difference in the incidence of serious
complications except localized bile duct dilatation between
the groups. Rare (<1%) ischemic cholecystitis occurred
in one patient in each group, probably due to regurgitation of
the chemoemulsion and embolic materials. The patient who
underwent C-TACE was treated conservatively and recovered
from cholecystitis. The patient who underwent DEB-TACE
was treated by percutaneous cholecystostomy and recovered.
Peri-tumoral parenchymal ischemic changes, other than overt
infarction, were observed in about 20% of patients in both
groups at the first follow-up imaging without any clinical significance.
Overt liver infarction around the tumor bed occurred
in about 3% of each group, and was managed conservatively without any intervention. Liver abscess formation in
infarcted tumor and the surrounding liver parenchyma occurred
in one patient in each group, and was treated by percutaneous
tube drainage and intravenous antibiotics. A higher
rate of localized bile duct dilatation was evident in the
DEB-TACE group (29/103, 28.2%) compared with the CTACE
group (7/115, 6.1%) (Pm<0.001) during the follow-up
imaging, but there were no clinical sequelae. Two patients in
the C-TACE group experienced progressive extensive whole
biliary tree necrosis that resulted in liver failure and mortality.
One patient in the DEB-TACE group experienced biliary tree
necrosis, but it was confined to a unilobar affected site without
progression. One mortality in the DEB-TACE group was
due to subsequent radiofrequency ablation (RFA) conversion
for the treatment of the residual viable portion after the initial
DEB-TACE; extensive portal vein thrombosis after the RFA
resulted in liver failure and mortality.
Table 5. Serious complications

C-TACE, conventional-trans-arterial chemoembolization; DEB-TACE, drug-eluting beads-trans-arterial chemoembolization; NS, not significant.
*Two mortalities in the C-TACE group were from extensive biliary necrosis resulting in liver failure, one mortality in the DEB-TACE group was due
to subsequent conversion to radiofrequency ablation (RFA) for the treatment of residual viable portion.
5. Target tumor response (Table 6)
The rates of target tumor response assessed by EASL criteria are summarized in Table 6. By the definition of all responses,
there was no significant difference between the two
modalities as an initial treatment choice at both the immediate
and 1-year assessment. Immediate complete response
rates in C-TACE and DEB-TACE groups were 81.7% and
77.7%, respectively. Immediate objective response rates in CTACE
and DEB-TACE groups were 94.8% and 96.1%, respectively.
One-year objective response rates in C-TACE and
DEB-TACE groups were 85% and 81.4%, respectively. Similar
rates of stable disease and progressive disease between the
groups were observed at the 1-year follow up.
Table 6. Target tumor response assessed by European Association for the Study of the Liver (EASL) criteria

C-TACE, conventional-trans-arterial chemoembolization; DEB-TACE, drug-eluting beads-trans-arterial chemoembolization; NA, not available.
6. Conversion to other treatment modalities
(Table 7)
At the study end time of 1-year, the conversion rate to other
treatment modalities such as surgical resection, RFA, or
exchange between C-TACE and DEB-TACE was significantly
higher in the DEB-TACE group (35/103, 40%) than in the CTACE
group (10/115, 8.7%) (P<0.001).
Table 7. Conversion to another treatment modality

C-TACE, conventional-trans-arterial chemoembolization; DEB-TACE,
drug-eluting beads-trans-arterial chemoembolization.
DISCUSSION
DEB-TACE has been reported to have a more stable pharmacokinetics profile than C-TACE in both animal and clinical
trials.6,7,16,17 An earlier trial comparing C-TACE and DEBTACE
showed that complications associated with the
procedure and the effusion of anticancer drugs and hepatic
dysfunction were less likely to occur in the DEB-TACE
group. In addition, the objective response rate and disease
control rate of HCC were found to be better in the DEBTACE
group.18 However, this was an early result of 6 months,
and no additional results have been reported since then. In an
earlier meta-analysis including a total of seven clinical studies
with 700 patients, DEB-TACE showed a significantly better
tumor response compared with C-TACE and better survival
for 1 and 2 years, in addition to a safer profile than C-TACE.19 In addition, in a more recent meta-analysis of nine clinical
studies with 866 patients, DEB-TACE also showed a higher
complete response rate and a higher overall survival rate as
well as a safer profile and fewer adverse events than CTACE.20 However, a couple of recent studies suggested different
conclusions. A systematic review that included four randomized
controlled trials, one uncontrolled prospective study and
one prospective case–control study, with a total of 652 patients,
suggested that DEB-TACE was associated with better
tumor response and potentially fewer adverse events, but
there was no survival benefit compared with C-TACE.21 Although
it was retrospective, a recent study that compared the
clinical outcomes of 250 patients (C-TACE, n=144; DEBTACE,
n=106) in terms of overall survial and time to progression
showed no significant difference in the median overall
survival (44.9 months in C-TACE group, 46.6 months in
DEB-TACE group), but a significantly longer median time to progression in the C-TACE group (13.3 months) compared
with the DEB-TACE group (10.8 months). The authors concluded
that DEB-TACE appeared to be safer, but was not superior
to C-TACE with regard to clinical efficacy.22 Thus, the factors to consider when comparing C-TACE
and DEB-TACE are both procedural safety and clinical outcome.
Currently, procedural safety and patient compliance
are clearly better for DEB-TACE than C-TACE, but clinical
outcome remains controversial.21-25 For safety issues such as severe intractable pain and bradycardia
during the procedure, PES, liver function changes, and
severe complications, we believe that the difference arises
from the basic different characteristics of the chemo-vehicles
and embolic materials of C-TACE and DEB-TACE. In CTACE,
severe ischemic pain occurs during the procedure because
of irritation to the peri-biliary plexus and liver capsule
due to the smaller chemo-laden lipiodol droplets, which are
an emulsion of the anticancer agent and lipiodol. In some
cases, blood pressure control and treatment of bradycardia
are required. In the case of DEB-TACE, pain is relatively rare
and tends to be vague and tolerable, and the vital signs remain
stable during the procedure. Basically, both C-TACE
and DEB-TACE are embolic procedures that cause deterioration
of liver function and PES. However, most of the reports
and meta-analyses have shown significantly higher fluctuations
in the liver function profiles and incidence of PES with
C-TACE compared to DEB-TACE. This result correlates with
preclinical studies of the pharmacokinetics profiles.6,7 A recent
report of a Korean multicenter registry of DEB-TACE
using DC beads presented a high rate of PES (73%) after the
first treatment cycle.26 The the low incidence of PES in the
DEB-TACE group in the current study might be due to the
small to medium sized single HCC cohort with a small extent
of involved liver. One report comparing the short-term safety
and efficacy of DEB-TACE and C-TACE using the superselective
TACE method showed no difference in overall toxicity
between the two groups.27 The authors explained that the reason
for this might be the superselective procedure. In our
study, we found significantly higher incidence of severe pain
and bradycardia, changes in liver enzymes, and PES in the CTACE
group than in the DEB-TACE group. This difference is probably because the chemo-lipiodol emulsion sufficiently
effluxes into the surrounding peri-tumoral portal venous system
when superselective TACE is performed. The most serious
complication of TACE is profound tumor and liver infarction
resulting in abscess formation and biliary tree
necrosis. An abscess can be managed by percutaneous drainage,
but extensive biliary tree necrosis might result in liver
failure and mortality. Biliary tree necrosis in C-TACE can be
progressive, whereas most of the bile duct injury in DEBTACE
is localized without clinical sequelae. This can be explained
by the fact that the smaller sized chemo-lipiodol
emulsion can be delivered to a fine peribiliary plexus, resulting
in progressive damage, but this is unlikely to occur with
the larger sized DEB microspheres. The reason why localized
bilateral duct dilatation occurs more frequently in DEBTACE
than C-TACE is probably that DEB-TACE has a stronger
embolic effect and therefore a profound liver parenchymal
ischemic volume change occurs in the tumor bed.
However, peribiliary plexus injury is unlikely to be severe in
DEB-TACE, as it is no longer progression. Progressive biliary
necrosis is thought to be more at risk in C-TACE. Because
drug-laden lipiodol is very small size, peribiliary plexus injury
can be induced, but DEB of more than 100 µm is less likely to
induce peribiliary plexus injury. One progressive biliary necrosis
occurred in the DEB-TACE group, not after DEBTACE,
but after RFA for residual viable portion. Regarding clinical outcome, it is hard to compare the data
since most of the patients were converted to other treatment
modalities during the follow-up based on institutional policy
or the individual clinician’s preference if there was any local
tumor recurrence, even with a very small viable portion. By
the end point, conversion to other therapies such as surgery,
RFA, adjunctive external beam radiation therapy, conversion
from DEB-TACE to C-TACE, and systemic chemotherapy or
molecular targeting agent occurred upon recurrence in almost
all patients. C-TACE can be performed as many times
as needed because of the small size of the chemo-lipiodol
emulsion, which can be delivered even to fine collaterals or
injured arteries. If local recurrence occurs again to less effectiveness
C-TACE through such collaterals or injured arteries,
then conversion to other therapies such as surgery or RFA should be decided. In contrast, for DEB-TACE, there is an
apparent limitation of repeat procedures. Since DEB microspheres
are permanent embolic materials, there is deprivation
of the native arteries and fine collateral formation; therefore,
large DEB microspheres cannot be delivered to fine collaterals
or damaged arteries. Such cases should be converted to CTACE
or RFA. For this reason, even when the initial treatment
is started with DEB-TACE, it is difficult to compare the
true clinical outcomes for the two modalities because the
same treatment is often not continued. A limitation of this study is that it is a retrospective casecontrolled
observation with immediate and early-term data at
1 year. Also, as mentioned above, the true clinical outcomes
could not be presented. In conclusion, DEB-TACE is certainly better than C-TACE
in terms of procedural safety as initial treatment in a very early
or early stage of HCC. However, a true comparative longterm
study of the differences between the two modalities for
tumor control and clinical outcome appears to be difficult.
Because the morphological classifications of HCC and clinical
liver function status are very diverse, it is advisable to know
the advantages and limitations of both C-TACE and DEBTACE
and to choose the appropriate treatment method for
each patient or even for the same patient during the course of
treatment.
FUNDING
The Scientific Research Fund of the Korean Liver Cancer
Study Group 2015
AUTHOR CONTRIBUTIONS
Kwang-Hun Lee, primary procedure operator, manuscript
writing; Seung-Moon Joo, primary procedure operator; Tae
Jun Yum, secondary procedure operator, statistic analysis;
Sang Hoon Jung, secondary procedure operator, data collection.
Conflicts of Interest
The authors have no conflicts to disclose.
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