REVIEW ARTICLE

Clinical Efficacy and Safety of Microwave Ablation Compared

to Radiofrequency Ablation in Hepatocellular Carcinoma
Patients: A Systematic Review and Meta-Analysis
of Randomized Controlled Trials
Rifaldy Nabiel Erisadana 1*, Yehuda Tri Nugroho Supranoto 1, Heni Fatmawati 1,2,
Irawan Fajar Kusuma 1,3, Adrian Wibisono 1, Putu Ayu Laksmi Lestari 1
1
Soebandi General Hospital, Faculty of Medicine University of Jember, Jember, Indonesia
2
Department of Radiology, Soebandi General Hospital, Faculty of Medicine University of Jember, Jember, Indonesia
3
Department of Internal Medicine, Soebandi General Hospital, Faculty of Medicine University of Jember, Jember, Indonesia

ARTICLE INFO ABSTRACT

Received : 22 November 2022 Background: Ablation modalities for the treatment of hepatocellular carcinoma (HCC) including
Reviewed : 08 December 2022 microwave ablation (MWA) and radiofrequency ablation (RFA) are clinically important due to
Accepted : 26 April 2023 their numerous advantages. Several trials showed inconsistent results regarding safety and
efficacy, making the comparison between MWA and RFA challenging. Therefore, this study aimed
Keywords: to enhance the evidence on treatment modalities regarding the clinical efficacy and safety of
hepatocellular carcinoma, MWA compared to RFA in HCC patients.
meta-analysis, microwave ablation,
radiofrequency ablation Methods: A systematic review and meta-analysis was conducted following the PRISMA guidelines.
Subsequently, a literature search was carried out by PubMed, ScienceDirect, and Google Scholar
for randomized controlled trials (RCTs) in HCC patients who passed through MWA compared to
RFA. Quantitative analysis of pooled risk ratio with a 95% confidence interval was performed using
Review Manager 5.4 software in a random-effects model or fixed-effects model forest plot.

Results: Based on 9 RCTs included in the analysis, there were insignificant different results in
terms of complete ablation rates (CA) [RR=1.01, 95%CI (0.99 to 1.03), p=0.47] and adverse events
(AE) [RR=1.15, 95%CI (0.88 to 1.50), p=0.31]. However, lower incidence of local tumor
progression (LTP) [RR=0.73, 95%CI (0.54 to 0.99), p=0.04], intrahepatic de novo lesions (IDL)
*Corresponding author: [RR=0.90, 95%CI (0.81 to 1.00), p=0.05], and extrahepatic metastases (EHM) [RR=0.65, 95%CI
Rifaldy Nabiel Erisadana (0.44 to 0.95), p=0.03] exhibited significant differences in MWA group.
Soebandi General Hospital,
Faculty of Medicine University Conclusions: This meta-analysis provided evidence that MWA and RFA had equivalent CA rates
of Jember, Jember, Indonesia and AE in HCC patients. However, MWA was considered superior to RFA due to a lower incidence
[email protected] of LTP, IDL, and EHM.

INTRODUCTION
systemic therapy [2]. Among these modalities, liver
Liver cancer is the third most common leading transplant remains the best curative option for early-stage
cause of mortality globally in 2020, following lung HCC, but its efficiency is limited by the scarcity of available
and colorectal cancer. Approximately 906,000 new donors [3]. Concerning surgical resection, proper patient
cases and 830,000 deaths were reported, with selection must be carefully considered with the result
hepatocellular carcinoma (HCC) accounting for 75–85% that only less than 5% meet the criteria [2].
[1]. Several treatment modalities are available for In cases where surgical resection or liver transplantation
HCC, including surgical resection, liver transplantation, is not feasible, thermal ablation techniques have emerged
percutaneous ethanol injection (PEI), radiofrequency as an alternative curative treatment for HCC patients,
ablation (RFA), microwave ablation (MWA), transarterial offering advantages with minimal invasiveness [4,5]. RFA
chemoembolization (TACE), and molecular targeted is well-known as a safe and effective thermal ablation for

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DOI: http://dx.doi.org/10.33371/ijoc.v17i3.988
MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

treating HCC, but it is prone to heat-sink effects, particularly Data extraction

when the tumor is located near the main biliary tree, Data extraction was carried out for all included
abdominal organs, or heart. Furthermore, MWA is a recent studies by two independent reviewers to obtain relevant
thermal ablation with higher temperature in a shorter time clinical outcomes, facilitating quantitative analysis.
to enhance local tumor controls, given less prone to heat- Several data were extracted from the included studies
sink effect, and be used in tumors adjacent to vessels [5]. such as year of publication, country, diagnosis and
The guidelines by the European Association for the criteria of HCC, number of patients, intervention, number
Study of the Liver (EASL) reported that MWA showed of nodules, tumor size, and number of Child-Pugh scores.
promising results for local control and survival [4]. Any controversies between data extraction were
However, these results were categorized as having low discussed with other authors.
evidence strength. Several studies that were recently
published, including randomized controlled trials (RCTs), Risk of bias assessment
also showed inconsistent outcomes regarding safety and The risk of bias assessment was performed using
efficacy, making the comparison between MWA and the Cochrane Risk of Bias 2 (ROB 2) tool [8]. This tool
RFA challenging. Therefore, this study aimed to enhance comprised several domains such as randomization
the evidence on treatment modalities using an updated sequence generation, allocation concealment,
systematic review and meta-analysis approach to provide performance, detection, attrition, reporting, and other
the best answer regarding the clinical efficacy and safety sources of bias. Each domain was graded as “low risk”,
of MWA compared to RFA in HCC patients. “unclear risk”, and “high risk” of bias. The risk of bias
assessment was conducted by two reviewers
METHODS independently and any difference in terms of grading
was discussed with other authors.
This systematic review and meta-analysis were reported
based on Preferred Reporting Items for Systematic Reviews Data synthesis and analysis
and meta-analysis (PRISMA) guidelines [6]. Meanwhile, The included studies were analyzed quantitatively
ethical clearance was not required for this study. using Review Manager (RevMan) 5.4 for meta-analysis
(Cochrane Collaboration, Oxford, UK) with 95% confidence
Database searching and study selection intervals (CI). The pooled risk ratio was used to calculate
A systematic literature search was carried out by the dichotomous outcomes. Based on heterogeneity, the
PubMed, Google Scholar, and ScienceDirect using some random effects model was employed when heterogeneity
keywords, which included MWA, RFA, and HCC. The was high (I2 ≥ 50%), while fixed effects model forest
review question for included studies was developed plots were used at a low value (I2 < 50%) [9].
following the PICOS framework (i) Population: patients
diagnosed with HCC or other liver malignancies, (ii) Publication bias
Intervention: MWA, (iii) Comparator: RFA, (iv) Outcomes: The publication bias was analyzed using Review
complete ablation rate (CA), local tumor progression Manager (RevMan) 5.4, which was visualized through
(LTP) is defined by the recurrence of the tumor with a funnel plots graph. The asymmetric shape observed
the same liver segment as the previously ablated, in the funnel plot suggested that publication bias was
intrahepatic de novo lesions (IDL), adverse events (AE), present, while the symmetrical shape of the funnel plot
and extrahepatic metastases (EHM) of HCC origin, and indicated the absence of publication bias.
(v) Study design: RCTs. The eligibility criteria for this
study included: 1) Meet the PICOS criteria, 2) Only RESULTS
articles written in English, and 3) Full-text articles were
available. The exclusion criteria consisted of studies in Studies selection
the form of a systematic review with or without meta- A PRISMA flowchart reported all studies’ selection
analysis, literature review, case report, series, non- processes, as presented in Figure 1. Based on databases
human subjects or in vitro studies, abstract-only papers searching from PubMed, Google Scholar, and Science
as preceding papers, conference, editorial, and author Direct, a total of 4522 articles were found. This was
response. The literature search was carried out in October followed by the elimination of duplication using Rayyan.
2022 without any year restriction. All results from ai and further screening through the review of the title
electronic databases were stored in Rayyan.ai to pass and abstract to remove irrelevant topics. Subsequently,
through the selection process [7]. Subsequently, two a total of 38 articles were checked for eligibility by full-
independent reviewers performed the selection process text screening. Quantitative synthesis and analysis using
based on title and abstract screening, followed by full- meta-analysis were performed in 9 articles.
text evaluation based on eligibility criteria. Any conflicts
during article selection were discussed with all authors.

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MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

Figure 1. PRISMA
flow diagram

Figure 2. Risk of bias

assessment based on RoB
2 tools

Study characteristics and risk of bias

Table 1 summarized all included RCTs with the and Egypt, and as well as 1 multi-country study involving
sample size varied between each study ranging from France and Switzerland. The risk of bias assessment
40 to 403 samples. Several nodules were reported was conducted using the Cochrane RoB 2. The blinding
between 20 to 265 in MWA groups and 20 to 251 in of participants and personnel domain was judged as a
RFA groups. The included studies were conducted in high risk of bias. This led to an elevated overall risk of
several countries, including 1 study in Japan, Italy, bias in included studies, as shown in Figure 2.
Hongkong, and Spain, 2 studies were reported in China

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 MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

Table 1. Characteristics of included studies

Number Mean/
Intervention Number of Child-
Study, year HCC Criteria of Mean/ Median
Nodules Pugh
(Country) and Diagnosis patients Median Age Size of
MWA RFA (≤3/>3 cm) A/B/C
(Male) Nodules

Shibata Solitary HCC MWA: MWA: Microwave 15-gauge MWA: MWA: MWA:
et al., nodule smaller 36 (24) 62.5 (52–74) electrode needle 46 (43/3) 2.2 19/17/-
2002 than 4 cm in RFA: RFA: 1.6 mm electrode RFA: (0.9–3.4) RFA:
(Japan) [10]
diameter or those 36 (26) 63.6 (44–83) in diameter with 8 or 10 48 (45/3) RFA: 21/15/-
with two or three and 25 cm hook-shaped 2.3
nodules less than in length expandable (1–3.7)
or equal to 3 cm connected electrode tines
in diameter was to 2450 MHz connected
confirmed in all microwave to a 460-kHz
patients with generator radiofrequency
ultrasonographically generator
(US) guided needle
biopsy

Qian Small HCC is MWA: MWA: 14-gauge 17-gauge MWA: MWA: NR

et al., defined single 22 (20) 52 ± 12 cooled-shaft internally 22 (NR/NR) 2.1 ± 0.4
2012 nodule with RFA: RFA: antenna cooled needle RFA: RFA:
(China) [11]
less than 3 cm 20 (19) 56 ± 11 connected electrode and 20 (NR/NR) 2.0 ± 0.5
diameter diagnosed to a 2450 MHz two dispersive
according to generator pads
the non-invasive with and connected to
diagnostic criteria maximum RF generator
power output with a
of 100 W maximum
power output
of 200 W

Di Vece Single liver tumor MWA: MWA: Performed Performed MWA: MWA: NR
et al., measuring ≥2 cm 20 (16) 63 (52–92) using AMICA using a 20 (NR/NR) 3.6
2014 to <7 cm RFA: RFA: MWA System generator RFA: (2.2–6.9)
(Italy) [12] in diameter 20 (13) 59 (47–83) consisting of with a 20 (NR/NR) RFA:
a generator maximum 3.2
with a output power (2.3–6.4)
frequency of 200 W
of 2,450 MHz and a 17G
and a internally
maximum cooled needle
power output electrode
of 110 W. with a 3-cm
exposed tip

Abdelaziz All patients with MWA: MWA: AMICA® GEM 18 gauge MWA: MWA: MWA:
et al., HCC with 3 or 66 (48) 53.6 ± 5 machine (200 mm) 76 (55/21) 2.9 ± 0.97 25/41/-
2014 fewer focal lesions RFA: RFA: operated at internally Cool RFA: RFA: RFA:
(Egypt) [13] (the largest not 45 (31) 56.8 ± 7.2 a frequency tip electrodes 52 (32/20) 2.95 ± 1.03 24/21/-
exceeding 5 cm of 2,450 MHz (Radionics®)
in size) who were through 14 connected
diagnosed and gauge (150 to a 500-KHz
managed according and 200 mm) radiofrequency
to the EASL cooled shift generator
guidelines electrodes

Yu et al., Early-stage HCC MWA: NR Cooled-shaft Cooled-shaft MWA: MWA: NR

2017 with tumor size 203 (NR) microwave radiofrequency 265 2.7 ± 1
(China) [14] ≤5 cm in diameter RFA: system system (190/75) RFA:
and tumor 200 (NR) RFA: 2.6 ± 1
number ≤3 251
(174/77)

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MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

Number Mean/
Intervention Number of Child-
Study, year HCC Criteria of Mean/ Median
Nodules Pugh
(Country) and Diagnosis patients Median Age Size of
MWA RFA (≤3/>3 cm) A/B/C
(Male) Nodules

Violi Patients with MWA: MWA: 15-gauge A 200 W MWA: MWA: MWA:
et al., chronic liver 71 (59) 68 (60–72) liquid-cooled generator 98 (NR/NR) 1.8 ± 0.65 57/14/-
2018 disease and HCC RFA: RFA: antenna and in the RFA: RFA: RFA:
(France and lesions of 4 cm 73 (62) 65 (59–73) a 2·45 GHz impedance 104 (NR/NR) 1.8 ± 0.71 53/20/-
Switzer­land) or smaller. generator control mode
[15]
HCC diagnosed with a power and a
by cross-sectional of 140 W clustered
imaging or biopsy were used internally
according to EASL cooled
or AASLD electrode
guidelines

Kamal Patients with MWA: 55 (42–80) 14 gauge (Angiodynamics MWA: MWA: MWA:
et al., definite HCC 28 (21) 200 mm RITA model® 34 (NR/NR) 3.25±0.92 22/6/-
2019 on top of liver RFA: disposable 1,500×) RFA: RFA: RFA:
(Egypt) [16]
cirrhosis related 28 (22) MWA probe generator and 34 (NR/NR) 3.28±0.91 22/6/-
to HCV whose HCC (AMICA probe RITA StarBurst
lesions are 3 MW) and XL needle
or less with a 2.45 GHz were used
no lesion more generator complying
than 5 cm (AMICA GEN® with the
AGN-H-1.2) manufacturer’s
instructions

Chong HCC is diagnosed MWA: MWA: Percutaneous Cool-tip RFA MWA: MWA: MWA:
et al., based on histology 47 (30) 63.0 (50–80) microwave needles of NR 3.1 (2–4.5) 39/7/1
2020 or the typical RFA: RFA: needle with various sizes RFA: RFA: RFA:
(Hong Kong) imaging 46 (38) 64.5 (42–85) various power NR 2.8 (2–5.5) 40/6/-
[17]
appearance and and duration
raised alpha-fetal settings
protein (AFP) with depending on
tumor size ≤5 cm tumor size
in diameter and
tumor number ≤3

Radosevic HCC or other MWA: MWA: 2.45 GHz A single MWA: MWA: MWA:
et al., liver malignancies 39 (22) 75 (46–93) MW ablation 14-gauge, 47 (NR/NR) 2.5 28/2/
2022 suitable for RFA: RFA: generator 3 cm long RFA: (1.5–4.0) NR
(Spain) [18] ablation are 38 (29) 67 (48–84) with a internally 50 (NR/NR) RFA: RFA:
assessed by maximum cooled 2.4 21/6/
cross-sectional output of electrode with (1.5–4.0) NR
imaging or biopsy 140 W two electrically
(according to BCLC and a cooled isolated
classification 1 or mini-choked expandable
ESMO guidelines). 14-gauge and conducted
Tumor number at antenna with a 200 W
presentation ≤ 3 generator
and the largest
tumor diameter
between 1.5
and 4 cm

MWA, microwave ablation; RFA, radiofrequency ablation, HCC; hepatocellular carcinoma; EASL, European Association for the Study of the Liver;
AASLD, American Association for the Study of Liver Diseases; HCV, hepatitis C virus: NR, not reported

Outcomes: complete ablation (CA) rates

A total of 9 studies were reported on complete [pooled RR = 1.01, 95%CI (0.99 to 1.03), p=0.47], with
ablation rates with 635/655 and 601/625 events in MWA low heterogeneity between studies observed (I2=0%),
and RFA groups, respectively. The results showed that as shown in Figure 3.
the pooled estimates did not show statistically significant

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MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

Outcomes: local tumor progression (LTP) Outcomes: extrahepatic metastases (EHM)

A total of 7 studies were reported on LTP with EHM, which was conducted by only two studies,
63/576 and 83/547 events in MWA and RFA groups, showed a statistically significant difference. The results
respectively. This quantitative analysis showed statistically indicated that MWA groups were lower with 38/363
significant differences, where LTP was lower in MWA events compared to RFA with 56/355 events [pooled
groups [pooled RR = 0.73, 95%CI (0.54 to 0.99), p=0.04], RR = 0.65, 95%CI (0.44 to 0.95), p=0.03], exhibiting low
and there was a mild heterogeneity (I2=45%), as heterogeneity (I2=0%), as shown in Figure 6.
presented in Figure 4.
Outcomes: adverse events (AE)
Outcomes: intrahepatic de novo lesions (IDL) A total of 8 studies were reported on AE with 72/547
A total of 4 studies were reported on IDL with and 62/529 events in MWA and RFA groups, respectively.
239/451 and 257/422 events in MWA and RFA groups, The results showed a significant difference between
respectively. This quantitative analysis showed that IDL the groups [pooled RR = 1.15, 95%CI (0.88 to 1.50),
was statistically significantly lower in MWA groups p=0.31], and mild heterogeneity in the analysis was
[pooled RR = 0.90, 95%CI (0.81 to 1.00), p=0.05]. observed (I2=44%), as presented in Figure 7.
Furthermore, the heterogeneity was low between groups
(I2=17%), as shown in Figure 5.

Figure 3. Forest plots and funnel plots in terms of complete ablation (CA) rates

Figure 4. Forest plots and funnel plots in terms of local tumor progression (LTP)

Figure 5. Forest plots and funnel plots in terms of intrahepatic de novo lesions (IDL)

Figure 6. Forest plots and funnel plots in terms of extrahepatic metastases (EHM)

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MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

Figure 7. Forest plots and funnel plots in terms of adverse events (AE)

DISCUSSION
A meta-analysis of 9 RCTs involving 998 HCC patients that the advantage might be related to the necrosis of
was conducted to enhance the evidence regarding the microsatellites in association with the wider area of
clinical efficacy and safety of MWA compared to RFA. necrosis due to MWA treatment. Similarly, Radosevic
Ablation therapy including MWA and RFA had been et al. [18] highlighted that MWA created larger ablation
selected as the best modality for the early and very zones than RFA.
early stages of HCC when the resection was infeasible Glassberg et al. [22] showed insignificant results in
and the liver donor transplantation was not suitable. terms of EHM with 1 RCT and 1 cohort study that were
Although several studies regarding efficacy and safety analyzed. Although this study obtained lower incidences
between MWA and RFA had been published, inconsistent of EHM in MWA treatment, the result should be
results were found, contributing to ongoing debates. interpreted with caution due to the inclusion of only
This up-to-date meta-analysis showed that there was 2 RCTs in the analysis. Yu et al. [14] reported EHM for
no statistically significant difference in terms of CA rates 1-year, 3-year, and 5-year were 1.6%, 5.9%, and 13.2%
between MWA and RFA. Meanwhile, the latest meta- for MWA compared to 2.2%, 11.2%, and 19.3% for RFA.
analysis by Dou et al. [19] including 7 RCTs and 26 The achievement of a larger ablation zone through
cohort studies reported that CA rates of MWA were MWA led to concerns about more complications,
higher than RFA. This study confirmed the previous including liver injury and potential impact on organs,
meta-analysis by Spiliotis et al. [21], which included 4 particularly vascular and biliary structures [24]. However,
RCTs and 11 observational studies. According to a these results aligned with the meta-analysis by Tan
previous report by Facciorusso et al. [20] on 7 RCTs, et al. [25], Spiliotis et al. [21], and Dou et al. [19],
MWA and RFA exhibited similar rates of complete tumor which refuted the significant difference between MWA
ablation. The theoretical advantages of MWA regarding and RFA treatment regarding adverse events. These
higher temperature and faster heating, larger ablation studies also reported that the highest incidence of
volume, and less heat-sink effect than RFA were adverse events was pain at the site of intervention about
associated with other indicators compared to CA rates. 42.9% in both MWA and RFA treatment [16]. The meta-
This study showed the advantages of MWA over analysis suggested that both the ablative therapies were
RFA regarding the reduction of LTP, IDL, and EHM. The safe with a low incidence of adverse events.
lower incidence of LTP after MWA treatment was in The systematic review and meta-analysis were
line with three previous meta-analyses by Glassberg et carried out using the latest literature search, focusing
al. [22], Spiliotis et al. [21], and Dou et al. [19], but in on clinically relevant outcomes, and yielding results with
contrast with Facciorusso et al. [20]. The study by Lin low heterogeneity. The meta-analysis involving only RCTs
et al. [23] involving 564 hepatic malignant tumors might help to empower the answer regarding the
showed that the heat-sink effect due to RFA treatment inconsistent results. However, the limitations of this study
was an important factor affecting the recurrence of consisted of the inclusion of articles on different follow-
hepatic malignant tumors. Furthermore, this analysis up times for the outcomes. Different types of MWA and
suggested that LTP was considered a more reliable RFA machine treatments that were used also affected
indicator for treatment efficacy than CA rates. the outcomes. The intervention and evaluation procedures
Intrahepatic de novo lesions also referred to as distant depended on the operators, contributing to variations
intrahepatic tumor progression or intrahepatic metastases in experiences and capabilities between the included
are beneficial to MWA treatment. This result was studies. Consequently, further RCTs with larger sample
contradictory to Spiliotis et al. [21], where extrahepatic sizes and various outcomes were urgently needed to
new tumors were discovered for distant recurrence provide high-quality evidence and enhance the robustness
analysis. A meta-analysis conducted by Facciorusso et al. of the current systematic review and meta-analysis.
[20] on only 2 RCTs for de novo lesion outcomes stated

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MWA versus RFA in HCC: A Meta-Analysis RIFALDY NABIEL ERISADANA, ET AL

CONCLUSIONS 10. Shibata T, Iimuro Y, Yamamoto Y, et al. Small

hepatocellular carcinoma: comparison of radio-
This meta-analysis provided valuable evidence frequency ablation and percutaneous microwave
indicating that MWA and RFA exhibited equivalent CA coagulation therapy. Radiology. 2002 May;223(2):
rates and AE in HCC patients. However, MWA was 331–7.
considered superior to RFA due to a lower incidence 11. Qian GJ, Wang N, Shen Q, et al. Efficacy of
of LTP, IDL, and EHM. microwave versus radiofrequency ablation for
treatment of small hepatocellular carcinoma:
DECLARATIONS experimental and clinical studies. Eur Radiol. 2012
Sep;22(9):1983–90.
Competing interest 12. Vece F Di, Tombesi P, Ermili F, et al. Coagulation
The authors declare no competing interest in this study. Areas Produced by Cool-Tip Radiofrequency Ablation
and Microwave Ablation Using a Device to Decrease
Acknowledgment Back-Heating Effects : A Prospective Pilot Study.
The authors wish to thank the Department of Radiology Cardiovasc Interv Radiol. 2014;37:723–9.
and Internal Medicine, Soebandi General Hospital 13. Abdelaziz A, Elbaz T, Shousha HI, et al. Efficacy and
Jember. survival analysis of percutaneous radiofrequency
versus microwave ablation for hepatocellular
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