Journal of Surgical Oncology 2012;106:322–326

Radiofrequency Ablation Combined With Systemic Chemotherapy in

Nasopharyngeal Carcinoma Liver Metastases Improves
Response to Treatment and Survival Outcomes

YING JIN,1,2 YU-CHEN CAI, PhD,2 YE CAO, MD,2 XIU-YU CAI,2 YU-TING TAN,2
YAN-XIA SHI, MD, PhD,2* AND WEN-QI JIANG, MD, PhD2*
1
Department of Medical Oncology, Zhejiang Cancer Hospital, China
2
State Key Laboratory of Oncology in South China, Department of Medical Oncology, Sun Yat Sen University Cancer Center, China

Background: Systemic chemotherapy is the major treatment modality for nasopharyngeal carcinoma (NPC) liver metastases. We investigated
the effectiveness of radiofrequency ablation (RFA) treatment, which has not been well explored in this disease.
Methods: One-hundred and thirty-four cases of NPC with liver metastases treated with chemotherapy, chemotherapy with RFA, or RFA alone
were retrospectively analyzed. Patient survival was evaluated by the log-rank test. Survival was analyses using the Kaplan–Meier method.
Cox multivariate analyses of clinicopathological features and different treatment approaches were conducted.
Results: Local response rates were 58% in the RFA group, 78% in the chemotherapy group and 93% in the chemotherapy with RFA group
(P < 0.001). Increased progression-free survival (PFS) and overall survival (OS) were observed in the chemotherapy with RFA group
(P < 0.001). Cox multivariate analysis indicated that the number of liver metastases (1 vs. >1), the dimension of the largest liver metastases
(
3 cm vs. >3 cm), evaluation of treatment (response vs. no response) and disease-free survival (
12 months vs. >12 months) were inde-
pendent prognostic factors.
Conclusions: RFA combined with chemotherapy is a promising treatment for NPC metastatic liver disease with improved local response,
PFS, and OS compared to current chemotherapy protocols.
J. Surg. Oncol. 2012;106:322–326. ß 2012 Wiley Periodicals, Inc.

KEY WORDS: liver metastases; nasopharyngeal carcinoma; radiofrequency ablation; systemic chemotherapy

INTRODUCTION PATIENTS AND METHODS

Nasopharyngeal carcinoma (NPC) is common in southern regions
of China, especially in Guangdong province [1,2]. NPC has the high-
est propensity of head and neck cancers to metastasize to distant
sites, which represents the major cause of death. Approximately 50%
of patients with NPC present with distant metastases [3,4]. Bone,
lung, liver, and distant lymph nodes are the most common metastasis
site [5], and patients with liver metastases have the worst prognosis
and shortest survival time [6]. Current management of NPC metastat-
ic disease is based on palliative systemic chemotherapy [7–10]. In
patients with colorectal liver metastases, surgical resection combined
with chemotherapy is the standard therapeutic approach, which po-
tentially cures metastatic disease; however, many factors limit the
overall usefulness of this technique [11,12]. Although surgical resec-
tion still remains the treatment of choice for primary and secondary
hepatic tumors, several local ablative therapeutic modalities have
emerged as reliable alternatives to resection or as adjuncts in oncol-
ogical treatment. Throughout the past two decades, the importance
of radiofrequency ablation (RFA) has continuously increased in the
treatment of localized primary or secondary cancers in the liver.
RFA is a minimally invasive technique, which employs high-energy
radio frequency waves to destroy tumors, and has gained consider-
able attention as an alternative to surgery in the treatment of hepato-
cellular and colorectal carcinoma metastases. RFA has the unique
advantages of a high rate of local control and low rate of treatment-
related complication [13–15]. The potential and survival benefit of
local treatments such as RFA in treatment of NPC liver metastases
has not been well characterized, prompting us to conduct a retro-
spective study. Clinical data from 134 patients with NPC metastatic
liver tumors was reviewed to compare the efficacies of chemotherapy
alone, RFA alone and chemotherapy with RFA.
Case Selection
A consecutive series of patients with liver metastases from NPC
were identified from the cancer registry database at Sun Yat-sen Uni-
versity Cancer Center (from January 1990 to December 2008). Inclu-
sion criteria were patients with pathologically confirmed NPC, liver
metastases determined by abdominal CT, fewer than three liver me-
tastases, the greatest dimension of liver metastases <5 cm, metasta-
ses limited to a single hepatic lobe, patients treated in our hospital
with complete clinical data and liver function of Child-Pugh class A
or B. Exclusion criteria were presence of other malignant tumors,
extra-hepatic metastases, liver function of Child-Pugh class C, bile
duct or major vessel invasion, and tumor proximity to vital structures
like vessels and bile duct. One hundred and thirty-four patients
were retrospectively enrolled and the clinicopathological features are
summarized in Table I.
Grant sponsor: National Eleventh Five Technology Major Project; Grant
number: 2008ZX09312-002; Grant sponsor: Sun Yat-sen Cancer Center.
All authors state that they have no conflicts of interest.
*Correspondence to: Yan-Xia Shi, MD, PhD and Wen-Qi Jiang, MD,
PhD, Department of Medical Oncology Cancer Center, Sun Yat-Sen
University, 651 Dongfeng East Road, Guangzhou 510060, China. Fax:
86-20-87343352. E-mail: shi_yx@sina.cn; jiang_wq@sina.cn
Received 30 June 2011; Accepted 14 December 2011
DOI 10.1002/jso.23034
Published online 23 January 2012 in Wiley Online Library
(wileyonlinelibrary.com).

ß 2012 Wiley Periodicals, Inc.

 RFA in Metastatic Liver NPC 323
TABLE I. Correlation Between Clinicopathologic Features and Different Treatment Modalities for 134 Patients With Liver Metastasis From NPC

Characteristic Cases (N) RFA N (%) Chemotherapy N (%) Chemotherapy þRFA N (%) P-value

Age 0.445
<45 years 58 16 (32%) 18 (45%) 16 (36%)
45 years 76 34 (68%) 22 (55%) 28 (64%)
Gender 0.830
Male 117 43 (86%) 36 (90%) 38 (86%)
Female 17 7 (14%) 4 (10%) 6 (14%)
Histology 0.729
WHO I 52 17 (34%) 17 (43%) 18 (41%)
WHO II 74 30 (60%) 20 (50%) 24 (55%)
WHO III 8 3 (6%) 3 (7%) 2 (4%)
Number of liver metastases 0.067
1 49 12 (24%) 18 (45%) 19 (43%)
>1 85 38 (76%) 22 (55%) 25 (57%)
The greatest dimension of liver metastases 0.680

3 cm 81 32 (64%) 22 (55%) 27 (61%)
>3 cm 53 18 (36%) 18 (45%) 17 (39%)
DFS 0.273

12 months 85 36 (72%) 24 (60%) 25 (57%)
>12 months 49 14 (28%) 16 (40%) 19 (43%)

The statistics was based on Kruska–Wallis H. P > 0.05 indicates no significant difference in the feature among the three treatment modalities.

Treatment Approach Statistical Analysis

All the treatments were the first-line therapy patients received
after developing liver metastases. Comprehensive consideration of
the patients, economic situation and their own choices were made
when the multidisciplinary team of our center selected the treatment
approach. Among the 134 patients, 40 underwent chemotherapy
alone, 50 underwent RFA alone and 44 underwent RFA combined
with chemotherapy. Chemotherapy regimens in the study were all
cisplatinum-based doublet which included: (i) cisplatin [25 mg/m2
intravenously (IV) on days 1–3 of a 21-day cycle] plus 5-fluorouracil
(500 mg/m2 IV on days 1–5 of a 21-day cycle); (ii) cisplatin (25 mg/m2
IV on days 1–3 of a 21-day cycle) plus paclitaxel (175 mg/m2 IV on
day 1 of a 21-day cycle).
RFA was performed percutaneously under local anesthesia and
sedation or general anesthesia. CT or ultrasound was used to guide
placement of the RF needle into the lesions to be treated by RFA.
Single/clustered needle electrode(s) with a 2 or 3 cm exposed tip
were used. Of the 44 patients who underwent chemotherapy concur-
rent with RFA, 37 patients received RFA followed by chemotherapy
and seven patients received chemotherapy followed by RFA.
Statistical analysis was performed using SPSS17.0. Survival was
calculated using the Kaplan–Meier method and log-rank test. Multi-
variate analysis was performed using the Cox proportional hazards
regression model. Short-term efficacy data and the relationship be-
tween different treatment approaches and clinicopathological factors
were analyzed using the Kruskal–Wallis H-test. Cox multivariate
was used to analyze patient clinicopathological features. Statistical
significance was defined as P < 0.05 using two-tailed tests.
RESULTS
Long-Term Treatment Efficacy
Improved PFS and OS were obtained in the chemotherapy with
RFA group compared to the RFA group, and also in the chemo-
therapy group compared to the RFA alone group (P < 0.001, Fig. 1,
Table II). OS rates in the chemotherapy with RFA group were im-
proved at year 1, 2, and 3 in the chemotherapy with RFA group,
compared to the RFA and chemotherapy alone groups (Table II).

Short-Term Treatment Efficacy

Evaluation Protocol and Follow-Up
Short-term efficacy was assessed based on the response evaluation
criteria in solid tumors (RECIST) version 1.1 criteria as complete
response (CR), partial response (PR), stable disease (SD), or progres-
sive disease (PD). CR and PR were regarded as treatment responses.
The efficacy was assessed at every two cycles of chemotherapy and
1 month after RFA by Spiral triphasic enhanced CT.
Long-term efficacy was evaluated by progression-free survival
(PFS) and overall survival (OS). PFS was defined as time from first
day of treatment to newly occurring metastatic lesion, recurrence, or
expansion of the primary lesion. OS was calculated from the first
day of treatment to death. Disease-free survival (DFS) was calculated
from completion of initial treatment to diagnosis of liver metastases.
Patients were followed up at 3-month intervals after treatment
until March 1, 2011. Abdominal ultrasonography or CT, serum EB-
virus measurement, and liver function tests were performed during
each visit. When intrahepatic recurrence was suspected, spiral CT
was performed.
Senventy-eight lesions (mean  SEM tumor size of 2.8 
1.0 cm) were found in the 40 patients who underwent chemotherapy
alone, compared with 86 lesions (2.6  0.7 cm) in 50 patients who
underwent RFA alone and 89 lesions (3.2  1.0 cm) in 44 patients
who underwent RFA combined with chemotherapy. Short-term effi-
cacy was assessable in all of the 134 patients enrolled. The local
response rate was significantly higher in chemotherapy with RFA
group, compared to the RFA or chemotherapy alone groups
(P < 0.001, Table III).
Local Recurrence Rate and Recurrence Patterns
The 1-year local recurrence rate was significantly lower in chemo-
therapy plus RFA group (36.4% by patients and 33.7% by tumors),
compared to the RFA alone group (52% by patients and 45.3% by
tumors) and chemotherapy alone group (60% by patients and 46.2%
by tumors) (P < 0.001). One year after treatment, in the chemother-
apy plus RFA group, 36.4% patients had local recurrence and 13.6%

Journal of Surgical Oncology

324 Jin et al.
TABLE III. Evaluation for Treatment of the 134 Patients With Liver
Metastases From NPC Treated by Different Treatment Modalities

Local controla

Treatment group Cases (N) CR PR SD PD CR þ PR (%)

RFA 50 7 22 16 5 58
Chemotherapy 40 4 27 5 4 78
Chemotherapy þ RFA 44 18 22 2 2 93

CR, complete response; PR, partial response; SD, stable disease; PD, progres-
sive disease.
CR and PR were regarded as treatment responses.
a
Local control was evaluated by RECIST criteria 1.1.

Fig. 1. Survival curves in 134 NPC liver metastases patients treated

with chemotherapy, RFA or RFA with chemotherapy (A) Kaplan–
Meier PFS curves. Mean PFS  SE (95% CI) was 6.2  0.5 (5.3–
7.2) months in the RFA group, 9.3  1.1 (7.1–11.5) months in the
chemotherapy group and 13.9  2.1 (9.9–17.9) in the RFA with che-
motherapy group, P < 0.001. B: Kaplan–Meier OS curves. Mean
OS  SE (95% CI) was 14.8  1.2 (12.5–17.0) months in the RFA
group, 20.0  2.2 (15.7–24.3) months in the chemotherapy group
and 30.6  2.6 (25.4–35.7) months in the RFA with chemotherapy
group, P < 0.001. [Color figure can be seen in the online version of
this article, available at http://wileyonlinelibrary.com/journal/jso]
patients had new lesions; in the RFA alone group 52% patients had
local recurrence and 34% patients had new lesions; in the chemo-
therapy alone group 60% patients had local recurrence and 7%
patients had new lesions.
Adverse Effects
Of the 94 patients who underwent RFA with or without chemo-
therapy, no deaths or severe complications, skin burn or liver failure
was observed in any patient. The major adverse effects directly relat-
ed to RFA treatment were acute pain in 36 patients (38.3%) con-
trolled by oral analgesic and fever lasting more than 3 days in 9
patients (9.6%), which recovered after antibiotic treatment. In one
patient (1.1%), a liver abscess developed and was successfully
treated with percutaneous needle aspiration and antibiotics.
Prognostic Factors for OS
Independent of treatment modality, Cox multivariate analysis in-
dicated short-term response to treatment significantly affected the
outcome of the patients with NPC liver metastases (OR ¼ 2.507,
95% CI ¼ 1.557–4.038, P < 0.001). Additionally, the presence of
more than one liver metastases (OR ¼ 1.572, 95% CI ¼ 1.061–
2.331, P ¼ 0.024), having liver metastases >3 cm (OR ¼ 1.950,
95% CI ¼ 1.345–2.826, P < 0.001) and DFS
12 months
(OR ¼ 0.689, 95% CI ¼ 0.478–0.993, P ¼ 0.046) were significantly
poorer prognostic factors for OS (Table IV). Patients who responded
to treatment had a 1-year OS rate of 79%, compared with 31% for
patients with no response to treatment (Fig. 2A). Patients with only
one hepatic lesion had a 1-year OS rate of 86%, compared with 59%
for patients with more than one hepatic lesion (Fig. 2B). Patients
with liver metastases >
3 cm had a 1-year rate OS rate of 83%,
compared with 54% in patients with liver metastases >3 cm
(Fig. 2C) Patients whose DFS was >12 months had a 1-year OS
rate of 78%, compared with 64% for patients whose DFS was

12 months (Fig. 2D).
DISCUSSION
NPC has the highest tendency to metastasize to distant sites
among head and neck cancer. About half of the patients with NPC
eventually failed treatment due to distant metastases, which represent
the major cause of death for NPC [3,4]. Of patients with distant
metastases, liver metastases presents the worst outcome and has the
shortest survival time [6,16]. Current therapy for patients who pres-
ent with hepatic metastases from NPC are palliatively systemic
chemotherapy consist of a platimum-based combination regimen.
Commonly used active agents alone or in combination include cis-
platin, carboplatin, paclitaxel, and gemcitabine [17,18]. Be different
from colorectal liver metastases having curable potentiality, once di-
agnosed liver metastases the patients with NPC are always incurable.
One of the major causes may be that the multidisciplinary treatment
in patient with hepatic disease from NPC is not well established
compared to in those with colorectal liver metastases [11,12,19].
Therefore, to improve survival of patients with NPC liver metastases
multimodal therapy is required. RFA plus chemotherapy is one
strategy.
RFA allows tumors or other tissue to be abated using high fre-
quency and is used to treat lung, liver, kidney and bone tumors [20–
22]. Recently, tumor RFA has gained interest and acceptance due to
high effectiveness and low complication rates [23–25]. The clinical
benefits of RFA in colorectal hepatic metastases has been well
investigated [26–28]; however, it has not been fully investigated in
treatment of NPC hepatic metastases.
To the best of our knowledge, this is the first study comparing the
efficacy of RFA in the treatment of NPC liver metastases. RFA com-
bined with chemotherapy is superior to chemotherapy alone, with an

TABLE II. Survival Rate, PFS, and OS of 134 Patients With NPC Liver Metastases Among the Three Different Treatment Groups

Survival rate (%) PFS (months) OS (months)

Treatment group 1 year 2 year 3 year Mean  SE (95%CI) Mean  SE (95% CI)

RFA 56 14 2 6.2  0.5 (5.3–7.2) 14.8  1.2 (12.5–17.0)

Chemotherapy 60 38 13 9.3  1.1 (7.1–11.5) 20.0  2.2 (15.7–24.3)
Chemotherapy þ RFA 91 61 36 13.9  2.1 (9.9–17.9) 30.6  2.6 (25.4–35.7)

95%CI, 95%confidence interval; PFS, progression-free survival; OS, overall survival.

Journal of Surgical Oncology


TABLE IV. Cox Regression Multivariate Analysis of Prognostic Factors
for NPC Liver Metastases
Item OR 95% CI for Exp(B) P
With no response to treatment 2.507 1.557–4.038 <0.01
Number of liver metastases >1 1.572 1.061–2.331 0.024
Greatest liver metastases 1.950 1.345–2.826 <0.01
dimension >3 cm
DFS >12 months 0.689 0.478–0.993 0.046
95% CI, 95% confidence interval.
increased response rate (P < 0.001) and prolonged PFS and OS
(P < 0.001), suggesting local RFA treatment combined with system-
ic chemotherapy has a synergistic anti-tumor effect which signifi-
cantly improves outcome. Similar observations have been reported
by Gan et al. [29] that RFA with chemotherapy reduced local recur-
rence in unresectable small hepatocellular carcinoma compared to
RFA alone and Lee et al. [30] that RFA combined with chemothera-
py improved survival of stage III/IV non-small-cell lung cancer
patients, compared to chemotherapy. In addition, tumor debulking
has already proven survival benefit in ovarian cancer [31], this study
Fig. 2. Survival curves in 134 NPC liver metastases patients strati-
fied by clinicopathological features. A: Kaplan–Meier OS curves
stratified by patient response to treatment. Patients who responded
had a 1-year OS rate of 79% compared with 31% for those with no
response to treatment, P < 0.001. B: Kaplan–Meier OS curves strati-
fied by number of liver metastases. Patients with only one hepatic
lesion had a 1-year OS rate of 86%, compared with 59% for those
with more than one hepatic lesion, P < 0.001. C: Kaplan–Meier OS
curves stratified by largest dimension of liver metastases. Patients
with liver metastases
3 cm had a 1-year OS rate of 83%, compared
with 54% in patients with a greatest dimension of >3 cm,
P < 0.001. D: Kaplan–Meier OS curves stratified by DFS. Patients
whose DFS was >12 months had a 1-year OS rate of 78% compared
with 64% in patients with DFS
12 months, P > 0.05. [Color figure
can be seen in the online version of this article, available at http://
wileyonlinelibrary.com/journal/jso]
Journal of Surgical Oncology
RFA in Metastatic Liver NPC 325
also suggests that RFA for tumor debulking provides a survival bene-
fit in NPC metastatic liver disease. The concept that NPC hepatic
metastases are incurable needs revaluation, and we suggest the cur-
rent treatment modality of palliative systemic chemotherapy should
be altered. As our data is based on a retrospective review, the effec-
tiveness of local treatments including RFA in combination with sys-
temic chemotherapy should be studied in additional clinical trials.
The mean response rate of distant metastatic NPC to traditional
platinum-based doublets is about 60–85% in various reports [32,33].
The local response rate to chemotherapy observed in this study was
in accordance with these reports. It is notable that improved response
rate, PFS and OS were observed in the chemotherapy alone group
compared to RFA alone treated patients (P < 0.05). These results
suggest that systemic chemotherapy should still be the basic treat-
ment modality for patients with metastatic NPC, and local treatment
such as RFA should be used as an effective adjunct of systemic che-
motherapy. Combination of these two treatment modality can pro-
duce better effect than any one of them alone. The synergistic anti-
tumor effect of RFA with systemic chemotherapy reflects the multi-
discipline principle.
This study demonstrates that a lack of response to treatment
(P < 0.001), more than one liver metastases (P ¼ 0.024), liver me-
tastases over 3 cm (P < 0.001), and DFS under 12 months
(P ¼ 0.046) are poor prognostic factors, which could be used as
reference factors to predict survival outcome for patients with liver
metastases from NPC, regardless of treatment modality.
In conclusion, in order to improve survival of patients with liver
metastases from NPC, multimodal treatment is urgently needed. As
we showed in this study, RFA plus chemotherapy is one of feasible
strategies. We demonstrated that percutaneous RFA is a safe, well-
tolerated intervention for hepatic metastases. RFA combined with
systemic chemotherapy in NPC liver metastases treatment may pro-
long survival. However, since surgical resection still remains the
treatment of choice for primary and secondary hepatic tumors, liver
resection plus chemotherapy should be also investigated in patients
with NPC liver metastases in the future. We anticipate that future
clinical trials will establish multi-disciplinary approaches to change
the currently incurable situation for patients with liver metastases
from NPC.
ACKNOWLEDGMENTS
This work was supported by the National Eleventh Five Technol-
ogy Major Project (2008ZX09312-002) and the Research Award
Fund for Outstanding Young Researchers in Sun Yat-sen Cancer
Center. We thank Elixigen Co. for the generous help in manuscript
revision.
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