CLINICAL INVESTIGATION INTERVENTIONAL ONCOLOGY

Lung Radiofrequency Ablation for the Treatment of UnresectableRecurrent Non-Small-Cell Lung Cancer After SurgicalIntervention

Hiroshi Kodama • Koichiro Yamakado • Haruyuki Takaki •

Masataka Kashima • Junji Uraki • Atsuhiro Nakatsuka • Motoshi Takao •

Osamu Taguchi • Tomomi Yamada • Kan Takeda

Received: 2 February 2011 / Accepted: 7 June 2011 / Published online: 6 July 2011

� Springer Science+Business Media, LLC and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2011

Abstract

Purpose A retrospective evaluation was done of clinical

utility of lung radiofrequency (RF) ablation in recurrent

non-small-cell lung cancer (NSCLC) after surgical

intervention.

Methods During May 2003 to October 2010, 44 consec-

utive patients (26 male and 18 female) received curative

lung RF ablation for 51 recurrent NSCLC (mean diameter

1.7 ± 0.9 cm, range 0.6 to 4.0) after surgical intervention.

Safety, tumor progression rate, overall survival, and

recurrence-free survival were evaluated. Prognostic factors

were evaluated in multivariate analysis.

Results A total of 55 lung RF sessions were performed.

Pneumothorax requiring pluerosclerosis (n = 2) and sur-

gical suture (n = 1) were the only grade 3 or 4 adverse

events (5.5%, 3 of 55). During mean follow-up of

28.6 ± 20.3 months (range 1 to 98), local tumor progres-

sion was found in 5 patients (11.4%, 5 of 44). The 1-, 3-,

and 5-year overall survival rates were 97.7, 72.9, and

55.7%, respectively. The 1- and 3-year recurrence-free

survival rates were 76.7 and 41.1%, respectively. Tumor

size and sex were independent significant prognostic fac-

tors in multivariate analysis. The 5-year survival rates were

73.3% in 18 women and 60.5% in 38 patients who had

small tumors measuring B3 cm.

Conclusion Our results suggest that lung RF ablation is a

safe and useful therapeutic option for obtaining long-term

survival in treated patients.

Keywords Interventional oncology �Radiofrequency ablation � Lung/pulmonary � Cancer

Introduction

In many countries, lung cancer is the leading cause of death

among all cancers [1]. Surgery is the ‘‘gold-standard’’ for

the treatment of early stage non-small-cell lung cancer

(NSCLC). However, tumor recurrence occurs in approxi-

mately half of patients who undergo surgery [2]. When

recurrence is limited to the lung, surgical intervention is

considered the best treatment to provide longer survival

[3]. Five-year survival rates have been reported as being

23–42% after repeat surgery in such patients [4]. However,

\30% of patients are surgical candidates because of pul-

monary insufficiency or presentation with advanced stage

at the time of recurrence [3]. Therefore, [70% of patients

with recurrent NSCLC receive chemotherapy and/or radi-

ation therapy. However, satisfactory survival rates have not

been achieved compared with those after surgical resection

[5]. Few patients survive [5 years (median survival

6.4–14.9 months) [3]. Therefore, it is crucial to explore

new treatments to boost survival in patients with unresec-

table recurrent NSCLC.

H. Kodama (&) � K. Yamakado � H. Takaki � M. Kashima �J. Uraki � A. Nakatsuka � K. Takeda

Department of Radiology, Mie University School of Medicine,

Tsu, Mie 514-8507, Japan

e-mail: h-kodama@clin.medic.mie-u.ac.jp

M. Takao

Department of Thoracic Surgery, Mie University School

of Medicine, Tsu, Japan

O. Taguchi

Department of Internal Medicine, Mie University School

of Medicine, Tsu, Japan

T. Yamada

Department of Translational Medicine, Mie University School

of Medicine, Tsu, Japan

123

Cardiovasc Intervent Radiol (2012) 35:563–569

DOI 10.1007/s00270-011-0220-0

Recently, radiofrequency (RF) ablation has been used

for the treatment of unresectable lung tumors. Several

studies have demonstrated its safety, feasibility, and good

anticancer effects [6]. However, it has not been well

investigated whether lung RF ablation is useful in treating

recurrent NSCLC after surgical intervention. This study

was conducted to evaluate, retrospectively, the clinical

utility of lung RF ablation for the treatment of postopera-

tive unresectable recurrent NSCLC.

Materials and Methods

Study Design

This retrospective study was approved by our Institutional

Review Board. The necessity of informed consent for

inclusion in this study was waived. Informed consent to

perform lung RF ablation was obtained from all patients

before lung RF ablation was performed.

Patients

During May 2003–October 2010, 44 consecutive patients

with recurrent NSCLC after surgical intervention received

curative lung RF ablation. All patients were judged by

thoracic surgeons not to be surgical candidates because of

their advanced age, cardiopulmonary insufficiency, or

tumor location. Patients’ backgrounds are listed in Table 1.

There were 26 men and 18 women with a mean age of

70.0 ± 9.6 years (range 48–84). The pathological stage at

surgery was stage I in 34 patients (77.3%, 34 of 44) and

stages II to IV in the other 10 patients (22.7%, 10 of 44).

Histological types were adenocarcinoma in 35 patients

(79.5%, 35 of 44), squamous cell carcinoma in 6 patients

(13.6%, 6 of 44), and the others in 3 patients (6.8%, 3 of

44). Recurrent lung tumors appeared at 33.4 ± 33.4

months (range 4–172) after resection of primary lesions, on

average, in the same side of the resected lung in 28 patients

(63.6%, 28 of 44) and in the opposite side in 16 patients

(36.4%, 16 of 44). On computed tomography (CT) images,

ground-glass opacity (GGO) component in recurrent tumor

was dominant in 11 patients (25.0%, 11 of 44), and solid

component was dominant in the other 33 patients (75.0%,

33 of 44). Although liver and spleen metastases were found

at the time of lung RF ablation in 1 patient (2.3%, 1 of 44),

she was included in this study because curative RF ablation

was performed for both of the metastases. The other 43

patients (97.7%, 43 of 44) had no extrapulmonary metas-

tases. All patients had new lung masses that appeared and

became larger in size during follow-up. The diagnosis was

established based on only serial lung CT studies in 6

patients (13.6%, 6 of 44) and on both CT and positron

emission tomography (PET) studies in 14 patients (31.8%.

14 of 44). Percutaneous lung biopsy was performed in the

other 24 patients (54.5%, 24 of 44). According to the

Table 1 Patient backgrounds

Patient characteristics (%)

No. of patients 44

Age (years)

Mean ± SD 70.0 ± 9.6

B65 14 (31.8)

[65 30 (68.2)

Sex

Male 26 (59.1)

Female 18 (40.8)

Stage at surgical resection

Stage I 34 (77.2)

Stage II–IV 10 (22.8)

Disease-free interval (years)

Mean ± SD 2.8 ± 2.8

B2 23 (52.3)

[2 21 (47.7)

Previous chemotherapy

No 33 (75.0)

Yes 11 (25.0)

Previous radiation therapy

No 41 (92.2)

Yes 3 (6.8)

Tumor characteristics (%)

Histological type

Adenocarcinoma 35 (79.5)

Others 9 (20.5)

Maximum tumor diameter (cm)

Mean ± SD 1.7 ± 0.9

B3 38 (86.4)

3.1–4.0 6 (13.6)

Location of tumor

Same side of resected lung 28 (63.6)

Opposite side of resected lung 16 (36.4)

No. of tumors

Single 41 (92.2)

Multiple 3 (6.8)

GGO-dominant type on CT images

No 33 (75.0)

Yes 11 (25.0)

Intrapulmonary metastasis by the criteria of Martini et al.

No 28 (63.6)

Yes 16 (36.4)

Intrapulmonary metastasis by the criteria of ACCP guideline

No 17 (38.6)

Yes 27 (61.4)

564 H. Kodama et al.: RF Ablation for Recurrent NSCLC

123

criteria by Martini et al. [7], or the criteria by the American

College of Chest Physicians (ACCP) Evidence-Based

Clinical Practice Guideline [8], recurrent tumors were

considered intrapulmonary metastasis in 28 patients

(63.6%, 28 of 44) and secondary primary lung cancer in 17

patients (38.6%, 17 of 44). Three patients had multiple

recurrent lung tumors (range 2–5); therefore, 51 lung tumors

with a mean maximum tumor diameter of 1.7 ± 0.9 cm

(range 0.6–4.0 cm range) underwent RF ablation.

Pretreatment Work-up

Routine physical examination, laboratory tests, pulmonary

function tests, and imaging studies, including a chest

radiograph; chest, abdomen, and pelvic CT; and brain

magnetic resonance imaging (MRI), were performed

before lung RF ablation in all patients. Using a multide-

tector-row CT scanner (Aquillion 64; Toshiba, Otawara,

Japan), whole-body CT images were obtained (Fig. 1A).

Then three-phase contrast-enhanced chest CT images were

also acquired at 20 and 40 s after initiation of contrast

medium injection. At 90 s after the initiation of contrast-

medium injection, whole-body contrast-enhanced CT

images were acquired. Contrast medium (Omnipaque 300;

Daiichi Sankyo, Tokyo, Japan) was injected by way of the

antecubital vein with an injection rate of 5 ml/s and an

injected dose of 100 ml. F-18 fluoro-deoxy-glucose (FDG)

PET/CT was performed in 24 patients (54.5%, 24 of 44)

whose CT finding was not typical of recurrence. When both

of the imaging findings were equivocal to determine

whether lung tumor was recurrent tumor, lung biopsy was

performed.

Lung RF Ablation

Lung RF ablation was performed on an inpatient basis.

Five interventional radiologists (K. Y., A. N., J. U., M. K.,

and H. T.) performed lung RF ablation with local anes-

thesia using lidocaine (Xylocaine; Astellas Pharma, Tokyo,

Japan). Patients were under moderate sedation using fen-

tanyl citrate (Phentanest; Daiichi Sankyo, Tokyo, Japan).

Antibiotics (cefazolin and cefamezion; Astellas Pharma)

were administered prophylactically before and for 2 days

after RF ablation. Real-time CT fluoroscopy (Asteion;

Toshiba) was used to place the internally cooled electrodes

(Cool-Tip RF Ablation System; Coviden, Mansfield, MA)

in the tumor. A 2-cm-exposed tip electrode was used in 11

patients (25.0%, 11 of 44) having tumors measuring

B1 cm, and a 3-cm-exposed tip electrode in the other 33

patients (75.0%, 33 of 44). The electrode was placed in the

center of the tumor when the tumor size measured B2 cm.

When the tumor size was[2 cm, the electrode was placed

sequentially at 2–3 different sites in the tumor based on

tumor size and shape (Fig. 1B). After the electrode was

connected with the generator (Series CC-1; Valleylab,

Boulder, CO), RF energy was applied for 12 min at each

site of the tumor using an impedance-control algorithm.

Technical success was defined as RF ablation completed

with a planned protocol and the tumor covered by GGO

immediately after RF ablation [9](Fig. 1B).

Complications

Complications were assessed based on the number of

ablation sessions and defined based on Common Termi-

nology Criteria for Adverse Events version 4.03 (Common

Terminology 2010) [10]. Any patient death within 30 days

of image-guided tumor ablation (grade 5 adverse event)

was addressed. Grade 3 or 4 adverse events were defined as

major complications. Grade 1 or 2 adverse events were

defined as minor complications.

Follow-Up

Follow-up was determined as time of death or last patient

visit through December 31, 2010. Patients were followed-

up by three interventional radiologists (A. N., J. U., H. T.),

one thoracic surgeon (M. T.), and one respiratory internist

(O. T.). Routine physical examination, laboratory tests, and

Fig. 1 A 75-year woman with recurrent lung adenocarcinoma.

A Axial CT image shows a lung tumor measuring 2.2 cm in the

right upper lung 33 months after the patient underwent resection of

lung adenocarcinoma. B RF ablation was performed using two RF

electrodes. C She has been alive for 4 years since RF ablation. The

treated tumor became smaller and has a cord-like shape

H. Kodama et al.: RF Ablation for Recurrent NSCLC 565

123

measurement of tumor marker levels were performed every

month, and chest, abdomen, and pelvic CT studies were

performed every 3 to 4 months (Fig. 1C). Furthermore,

PET/CT studies were performed every 6 to 12 months.

Two diagnostic radiologists (H. K. and K. T.), who had

interpreted the technical success of RF ablation and local

tumor progression, also evaluated the CT and PET/CT

images. Local tumor progression was defined as the

appearance of enhanced nodule on CT images or signifi-

cant FDG uptake around the ablated tumor on PET/CT

images. Local tumor progression was treated again by lung

RF ablation when the maximum tumor diameter was

B4.0 cm and the tumors were not faced to the large vessels

and the lung hilum.

Assessment and Statistical Analysis

Survival was calculated from the time of lung RF ablation.

Cumulative overall and recurrence-free survival curves

were generated according to the Kaplan–Meier method.

Prognostic factors were evaluated by multivariate analysis

using stepwise Cox proportional hazard model.

Pretreatment baselines listed in Table 1 were used for

covariates for prognostic factors. The primary local tumor

progression curve was generated using the Kaplan–Meier

method. The secondary local tumor progression curve was

also generated taking into the result of repeat lung RF

ablation used for the control of local tumor progression.

Data are expressed as means ± SDs, and P \ 0.05 was

inferred as statistically significant. Statistical analyses were

performed using software (SPSS for Windows, version 15

[SPSS, Chicago, IL]).

Results

RF Ablation

In all, 55 lung RF ablation sessions were performed. The

RF electrodes were placed into all 51 tumor targets with

completion of the planned ablation protocol completed.

However, 1–2 RF ablations were added because GGO did

not cover the treated tumor completely in 8 tumors (15.7%,

8 of 51). Additional RF ablation was performed in 6

patients (14.3%, 6 of 42) having tumors B2 cm and in 2

patients (22.2%, 2/9) having tumors[2 cm. Therefore, the

technical success rate of RF ablation was 82.4% (42 of 51).

Complications

No death (grade 5 adverse event) was related to the RF

procedures (0%, 0 of 55). Pneumothorax developed during

19 of 55 RF sessions (34.5%, 19 of 55). Among these 19

sessions, surgical pleural suture was used in 1 session

(1.8%, 1 of 55), and pluerosclerosis was necessary in 2

sessions (3.6%, 2 of 55). Pneumothorax was cured by only

chest-tube placement in 11 sessions (20.0%, 11 of 55) and

abated with no treatment in the other 5 sessions (9.1%, 5 of

55). Self-limiting pulmonary hemorrhage and pleural

effusion occurred, respectively, during 3 (5.5%, 3 of 55)

and 3 (5.5%, 3 of 55) sessions. No other complications

were noted. Consequently, minor (grades 1 and 2 adverse

events) and major complication (grades 3 and 4 adverse

events) rates were, respectively, 40.0% (22 of 55) and 5.5%

(3 of 55).

Local Tumor Progression

Mean follow-up was 28.6 ± 20.3 months (range 1–98).

Local tumor progression was found in 5 patients (11.4%, 5

of 44). The 1-, 3- and 5-year primary local tumor pro-

gression rates were 5.4% (95% confidence interval [CI]

1.4–19.9), 14.2% (95 CI 1.8–27.6), and 42.8% (95% CI,

12.2–91.0) (Fig. 2), respectively. Local tumor progression

was ablated again by repeat RF ablation in 4 of the 5

patients (80.0%). Ablated tumors were controlled after the

second RF ablation in 3 of the 4 patients. However, one of

them experienced local tumor progression again. The fifth

patient was administered no treatment because of poor

general condition at the time of local tumor progression.

Therefore, treated tumors were controlled in 96.1% (49 of

51) of the patients by the end of the follow-up. Each of the

0

20

40

60

80

100

Loc

al tu

mor

pro

gres

sion

rat

e (%

)

0 1 2 3 4 5 6 7Follow-up period (year)

Primary local tumor progression rate

Secondary local tumor progression rate

Fig. 2 Cumulative initial and secondary local tumor progression rate.

Five of 36 patients (11.4%, 5 of 44) experienced local tumor

progression. The 1-, 3- and 5-year primary local tumor progression

rates were 5.4% (95% CI 1.4–19.9), 14.2% (95% CI 1.8–27.6), and

42.8% (95% CI 12.2–91.0) Three of five tumors with local tumor

progression were controlled by repeat RF ablation, and treated tumors

were well controlled in 96.1% (49 of 51) of cases. Each of the 1-, 3-

and 5-year secondary local tumor progression rates was 5.4% (95%

CI 1.4–19.9)

566 H. Kodama et al.: RF Ablation for Recurrent NSCLC

123

1-, 3- and 5-year secondary local tumor progression rates

was 5.4% (95% CI 1.4–19.9) (Fig. 2).

Survival and Prognostic Factors

Nine patients (20.5%, 9 off 44) died. Three patients died

from tumor progression, 5 patients from pneumonia, and 1

patient from cerebrovascular attack. The 1-, 3-, and 5-year

overall survival rates were 97.7% (95% CI 85.6–99.7),

72.9% (95% CI 55.1–90.7), and 55.7% (95% CI

29.7–81.6), respectively (Fig. 3). Recurrences were found

in 19 patients (43.2%, 19 of 44) in total. Of 5 patients with

local tumor progression, new lung tumors emerged in the

nontreated lung parenchyma in 3 patients. New lung

tumors developed in another 12 patients. Of them, 2

patients had metastases other than lung: There were liver

metastases in 1 patient and brain, lymph node, and liver

metastases in 1 patient. Nodal metastases were found in the

18th patient, and bone metastasis and carcinomatous

pleuritis were fund in the 19th patient. The 1- and 3-year

recurrence-free survival rates were 76.7% (95% CI

63.2–90.1) and 41.1% (95% CI 22.0–60.3), respectively

(Fig. 4).

Tumor size and sex were independent significant pre-

dictors in the multivariate analysis (Table 2). The 5-year

survival rates were 73.3% (95% CI 24.3–93.4) in 18

women and 60.5% (95% CI 32.5–88.4) in 38 patients who

had small tumors measuring B3 cm (Figs. 5, 6).

Discussion

The present study showed that lung RF ablation is a fea-

sible and safe therapeutic option for the treatment of

recurrent NSCLC. In this study, the RF electrode was

placed at the planned site, and GGO covered the tumor in

84.3% of tumors (42 of 51). Although additional RF

electrode placement was necessary in 15.7% (9 of 51) of

tumors, complete tumor ablation was achieved in all cases.

Pneumothorax was the only major complication. The

incidence of pneumothorax requiring chest-tube placement

has been reported as occurring during 0–21% of lung RF

ablation sessions [11]. In the present study, although most

pneumothorax occurring after lung RF ablation was minor,

the incidence of pneumothorax requiring chest-tube

placement (25.4%, 14 of 55) seems to be comparable with

or relatively higher than in previous reports. Okuma et al.

[12] reported that previous pulmonary surgery is a risk

factor for pneumothorax.

The local tumor progression rate was 11.4% (5 of 44) in

the present study. It is noteworthy that even after local

tumor progression, repeat RF ablation was performed in

80% (4 of 5) of the recurrent tumors and decreased the

secondary local tumor progression rate. Lower invasive-

ness appears to enable repeat lung RF ablation. Given that

none of our patients were surgical candidates, our results

showed that lung RF ablation has the possibility to provide

nonsurgical candidates with survival benefit. Good local

tumor control seems to contribute to prolonged survival.

Prognostic factors identified in the present study are

almost identical to those reported for surgical intervention

[13]. Tumor size is an important prognostic factor in

NSCLC patients. The larger the tumor becomes, the greater

the incidence of nodal or vessel invasion, which leads to

local tumor progression and/or distant metastasis [14].

Tumor size has been also a prognostic factors in RF

0

20

40

60

80

100

Ove

rall

surv

ival

rat

e (%

)

0 1 2 3 4 5 6 7

Follow-up period (year)

2235 27 115

Patients at risk44 1

Fig. 3 Overall survival rates. The 1-, 3-, and 5-year overall survival

rates were 97.7% (95% CI 85.6–99.7), 72.9% (95% CI 55.1–90.7),

and 55.7% (95% CI, 29.7–81.6), respectively

Rec

urre

nce

free

sur

viva

l rat

e (%

)

Follow-up period (year)

1326 26

Patients at risk

44

0

20

40

60

80

100

0 1 2 3 4 5 6 7

Fig. 4 Recurrence-free survival rates. The 1- and 3-year recurrence-

free survival rates were 76.7% (95% CI 63.2–90.1) and 41.1% (95%

CI, 22.0–60.3), respectively

H. Kodama et al.: RF Ablation for Recurrent NSCLC 567

123

ablation when treating both NSCLC and lung metastases

[15]. Female sex is a well-known better prognostic factor in

NSCLC patients who undergo surgery. Hormones and

lifestyle habit are considered to give women longer sur-

vival [16].

Limitations

This study has some limitations. The first is its retrospec-

tive nature. The second is the small number of patients.

Third, we did not perform lung biopsy in all patients and

did not strictly distinguish between recurrence of the ori-

ginal lung cancer and development of a new lung cancer. In

this study, survival was identical whether the recurrent

tumor was an intrapulmonary metastasis or a second pri-

mary cancer. Martini et al. reported that the distinction

between a new lung cancer and recurrence of the original

lung cancer is not as important as determing that the tumor

can be treated with curative intent. Despite these limita-

tions, our encouraging results suggest a useful framework

for future prospective studies.

Conclusion

In conclusion, lung RF ablation is a safe and effective

treatment in patients with recurrent NSCLC. RF ablation

can be the alternative therapeutic methods to surgery in

non-surgical candidates.

Conflict of interest None.

References

1. Youlden DR, Cramb SM, Baade PD (2008) The international

epidemiology of lung cancer: geographical distribution and sec-

ular trends. J Thorac Oncol 3(8):819–831

2. Moldvay J, Scheid P, Wild P et al (2000) Predictive survival

markers in patients with surgically resected non-small cell lung

carcinoma. Clin Cancer Res 6(3):1125–1134

3. Sugimura H, Nichols FC, Yang P et al (2007) Survival after

recurrent nonsmall-cell lung cancer after complete pulmonary

resection. Ann Thorac Surg 83(2):409–418

4. Asaph JW, Keppel JF, Handy JR Jr et al (2000) Surgery for

second lung cancers. Chest 118(6):1621–1625

5. Lamont JP, Kakuda JT, Smith D et al (2002) Systematic post-

operative radiologic follow-up in patients with non-small cell

lung cancer for detecting second primary lung cancer in stage IA.

Arch Surg 137(8):935–940

6. Yamakado K, Inoue Y, Takao M et al (2009) Long-term results of

radiofrequency ablation in colorectal lung metastases: Single

center experience. Oncol Rep 22(4):885–891

7. Martini N, Melamed MR (1975) Multiple primary lung cancers.

J Thorac Cardiovasc Surg 70(4):606–612

8. Rubins J, Unger M, Colice GL (2007) Follow-up and surveillance

of the lung cancer patient following curative intent therapy:

Table 2 Results of multivariate analysis

Hazard ratio 95% CI P

Tumor size [3 cm 12.37 4.63–33.02 0.01

Sex (female) 0.08 0.03–0.23 0.02

Fig. 5 Overall survival based on sex. Female sex is a significantly

better prognostic factor. The 1-, 3-, and 5-year overall survival rates

were 100%, 91.7% (95% CI 53.6–98.8), and 73.3% (95% CI

24.3–93.4), respectively, in female patients. The 1-year and 3-year

overall survival rates, as well as median survival time, were 96.2%

(95% CI 75.1–99.8) and 53.0% (95% CI 23.3–82.7) and 38.4 months,

respectively, in male patients

Fig. 6 Overall survival based on tumor size. Small tumor size

(B3.0 cm) is a significantly better prognostic factor. The 1-, 3-, and

5-year overall survival rates were 100%, 79.8% (95% CI 61.8–97.8),

60.5% (95% CI 32.5–88.4), respectively, in patients with tumors

measuring B3.0 cm. The 1-year and 3-year overall survival rates, as

well as median survival time, were 83.3% (95% CI, 27.4–97.5%) and

31.3% (95% CI, 1.3–73.3%), and 27.8 months, respectively, in

patients with tumors measuring 3.1–4.0 cm

568 H. Kodama et al.: RF Ablation for Recurrent NSCLC

123

ACCP evidence-based clinical practice guideline (2nd edition).

Chest 132(Suppl 3):355S–367S

9. Goldberg SN, Grassi CJ, Cardella JF et al (2009) Image-guided

tumor ablation: standardization of terminology and reporting

criteria. J Vasc Interv Radiol 20(Suppl 7):S377–S390

10. Common Terminology Criteria for Adverse Events (CTCAE)

Version 4.0 (2010). The National Cancer Institute, Bethesda

11. Hiraki T, Tajiri N, Mimura H et al (2006) Pneumothorax, pleural

effusion, and chest tube placement after radiofrequency ablation of

lung tumors: incidence and risk factors. Radiology 241(1):275–283

12. Okuma T, Matsuoka T, Yamamoto A et al (2008) Frequency and

risk factors of various complications after computed tomography-

guided radiofrequency ablation of lung tumors. Cardiovasc

Intervent Radiol 31(1):122–130

13. Goya T, Asamura H, Yoshimura H et al (2005) Prognosis of 6644

resected non-small cell lung cancers in Japan: A Japanese lung

cancer registry study. Lung Cancer 50(2):227–234

14. Rami-Porta R, Crowley JJ, Goldstraw P (2009) The revised TNM

staging system for lung cancer. Ann Thorac Cardiovasc Surg

15(1):4–9

15. Simon CJ, Dupuy DE, DiPetrillo TA et al (2007) Pulmonary

radiofrequency ablation: long-term safety and efficacy in 153

patients. Radiology 243(1):268–275

16. Brundage MD, Davies D, Mackillop WJ (2002) Prognostic fac-

tors in non-small cell lung cancer: a decade of progress. Chest

122(3):1037–1057

H. Kodama et al.: RF Ablation for Recurrent NSCLC 569

123