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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 14  |  Issue : 4  |  Page : 764-771

Computed tomography-guided percutaneous microwave ablation for treatment of peripheral ground-glass opacity–Lung adenocarcinoma: A pilot study


1 Department of Oncology, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, China
2 Department of Interventional Therapy, The First Affiliated Hospital of Fujian Medical University, Fuzhou, China
3 Department of Interventional Therapy, The Second Affiliated Hospital of Soochow University, Suzhou, China
4 Department of Oncology, Teng Zhou Central People's Hospital Affiliated to Jining Medical College, Tengzhou, China
5 Department of Oncology, Dezhou City People's Hospital, Dezhou, China
6 Department of Oncology, Weifang People's Hospital Affiliated to Weifang Medical College, Weifang, China
7 Interventional Center, Sun Yat-sen University Cancer Center, Guangzhou, China
8 Interventional Treatment Center, The Second Hospital Affiliated to Shandong University, Jinan, China

Date of Web Publication27-Jun-2018

Correspondence Address:
Xin Ye
Department of Oncology, Shandong Provincial Hospital Affiliated to Shandong University, Jinan 250014
China
Zhengyu Lin
Department of Interventional Therapy, The First Affiliated Hospital of Fujian Medical University, Fuzhou 350005
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_269_18

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 > Abstract 


Purpose: The purpose of the study is to retrospectively evaluate the safety and efficacy of microwave ablation (MWA) for the treatment of ground-glass opacity (GGO)–lung adenocarcinoma.
Materials and Methods: From December 2013 to June 2017, a total of 51 patients (22 males and 29 females, mean age of 69.4 ± 10.1 years) were included in this study, with 51 lung adenocarcinoma lesions showing GGO (mean long-axis diameter of 18.7 ± 6.05 mm). They received a total of 52 sessions of percutaneous computed tomography-guided (CT-guided) MWA. First, lung adenocarcinoma with GGO was histologically defined by needle biopsy under the guidance of CT. Second, the efficacy of CT-guided MWA was analyzed, including the feasibility, safety, 3 years local progression-free survival (LPFS), 3 years disease-specific survival, and 3 years overall survival (OS). Final, complications after MWA were also summarized.
Results: The technical success rate was 100%, without MWA procedure-related death. At the median follow-up period (27.02, range: 7–45 months), the rates of 3 years LPFS, cancer-specific survival, and OS were 98%, 100%, and 96%, respectively. The complications after MWA included pneumothorax (48.1%, 25/52), hemoptysis (28.8%, 14/52), pleural effusion (23.1%, 12/52), and pulmonary infection (7.7%, 4/52).
Conclusions: CT-guided percutaneous MWA was a feasible, safe, and effective therapeutic approach for treating GGO–lung adenocarcinoma.

Keywords: Ground-glass opacity, lung cancer, microwave ablation


How to cite this article:
Yang X, Ye X, Lin Z, Jin Y, Zhang K, Dong Y, Yu G, Ren H, Fan W, Chen J, Lin Q, Huang G, Wei Z, Ni Y, Li W, Han X, Meng M, Wang J, Li Y. Computed tomography-guided percutaneous microwave ablation for treatment of peripheral ground-glass opacity–Lung adenocarcinoma: A pilot study. J Can Res Ther 2018;14:764-71

How to cite this URL:
Yang X, Ye X, Lin Z, Jin Y, Zhang K, Dong Y, Yu G, Ren H, Fan W, Chen J, Lin Q, Huang G, Wei Z, Ni Y, Li W, Han X, Meng M, Wang J, Li Y. Computed tomography-guided percutaneous microwave ablation for treatment of peripheral ground-glass opacity–Lung adenocarcinoma: A pilot study. J Can Res Ther [serial online] 2018 [cited 2019 Nov 20];14:764-71. Available from: http://www.cancerjournal.net/text.asp?2018/14/4/764/235084




 > Introduction Top


Lung cancer screen through low-dose thoracic computed tomography (CT) has been performed since the 1990s, which has been gradually applied in worldwide.[1],[2] With the increasing CT screen, lung lesions with ground-glass opacity (GGO) have been often detected with the chest CT by accident. Usually, small lung lesions with GGO could be followed up with periodic CT. However, some lung lesions with GGO have been suspected as invasive adenocarcinoma, even if they were still small.[3],[4],[5] According to 2018 National Comprehensive Cancer Network Guideline of Lung Cancer Screening [6] or Fleischner society lung cancer treatment strategy guide,[7] surgical resection would be considered if pure GGO was observed to increase in size, density, or solid components. However, the selection of surgery type has been controversial. In addition, many patients with early-stage lung cancers could not be removed surgically for various reasons (such as multifocal lesions and cardiorespiratory failure). Therefore, many novel and local treatments have been emerging. Recently, local thermal ablation, as a precise and minimally invasive technique, has been increasingly applied to treat early-stage lung cancer.[8],[9],[10],[11],[12],[13],[14],[15]

Microwave ablation (MWA) is one of the local thermal ablation techniques, which has been applied to treat primary or metastatic lung tumors locally.[16],[17],[18],[19],[20],[21],[22] In this study, the safety, outcomes, and complications of MWA as an alternative approach for treating GGO–lung adenocarcinoma were retrospectively evaluated.


 > Materials and Methods Top


General information

During December 2013 and June 2017, a retrospective, multicenter study was conducted at either sites including Shandong Provincial Hospital Affiliated to Shandong University, the First Affiliated Hospital of Fujian Medical University, the Second Affiliated Hospital of Soochow University, Teng Zhou Central People's Hospital Affiliated to Jining Medical College, Dezhou City People Hospital, Weifang People's Hospital Affiliated to Weifang Medical University, Sun Yat-sen University Cancer Center, and the Second Hospital affiliated to Shandong University. This study enrolled 51 patients (22 males and 29 females; mean age of 69.4 years, range: 42–83 years) with 51 lung adenocarcinoma lesions showing GGO (mean long-axis diameter of 18.7 mm). A total of 52 percutaneous CT-guided MWA sessions were conducted including one repeated session due to the local progression. The patient and GGO characteristics were listed [Table 1].
Table 1: 51 case ground-glass opacity patient and tumor characteristics

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GGO was defined with a thin-section CT (TSCT) scan, as increased hazy opacities in the lung parenchyma with preservation of the bronchial structures and vascular margins.[23],[24] The diameter of the tumor (T) was defined as the largest axial diameter of the lesion on the lung window setting. The axial diameter of consolidation (C) on the lung window setting was also measured. The consolidation was defined as an area with increased opacification that completely obscured the underlying bronchial structures and vascular markings.[25],[26] All the preselected lung–GGO lesions were histologically adenocarcinoma, which was confirmed by needle biopsy under CT guidance before MWA. Positron emission tomography/CT scanning was performed in 18 patients before MWA, without any abnormal accumulation of 18 F-fluorodeoxyglucose. Typical classification of GGO is based on the findings of TSCT was as follows: pure GGO, part-solid GGO, and solid GGO.[25] In all involved lesions, thirty-four (34/51) were pure GGO, and seventeen (17/51) were part-solid GGO (C/T ≤50%). All patients were evaluated and consulted by an interdisciplinary group, consisting of a thoracic surgeon, radiation oncologist, radiologist, and medical oncologist.

The patients met the following criteria were enrolled in this study. Inclusion criteria: (1) a pulmonary lesion with a GGO (C/T ≤ 50%) on TSCT images (slice with the thickness of 1 mm or sub mm) before MWA, which could not be detected on CT scans in the mediastinal window setting; (2) GGO lesion size of ≤30 mm, single lesion; (3) medically intolerable to surgery due to poor lung functions (forced expiratory volume 1 [FEV1] <1 L, FEV1 z% <50%, maximum voluntary ventilation 50%), renal or heart dysfunction and other comorbid medical conditions (such as severe diabetes); (4) refused surgery; (5) no abnormal coagulability, platelet count ≥100 × 109, and (6) Eastern Cooperative Oncology Group performance status of ≤2. Exclusion criteria: the patients received previous therapy to the target lesion, or with regional lymph node metastasis or distant metastasis. Anticoagulant therapy and/or antiplatelet agents should be withdrawn for at least 5–7 days before the ablation procedure. The patients were informed in detail about the risks and benefits associated with MWA treatment. The written informed consent for the ablation procedure was obtained from all the patients. Ethics approval to conduct this study was obtained by the Institutional Review Board of all the sites.

Ablation protocol

MWA was conducted at the GGO sites under the guidance of percutaneous CT. A lightspeed 64 V spiral CT machine (GE) or a Siemens SOMATOM Sensation 64 CT scanner (Siemens) or a NeuViz 16 Platinum (Neusoft) was applied for scanning. MTC-3C MWA system (Vison-China Medical Devices R & D Center, CFDA Certificated No.: 20153251978), or KY-2450B MWA system (CANYOU Medical Inc., CFDA Certificated No.: 20153251727), or ECO-100A1 MWA system (ECO Medical Instrument Co., Ltd. CFDA Certificated No.: 20173251268) was applied for performing MWA. The microwave emission frequency was 2.450 ± 50 MHz. The adjustable output level of the continuous wave was ranged from 0 to 100 W. There was with a long-tapered end on the microwave antenna, with the effective length of 100–180 mm and an outer diameter of 14–19 G. A water circulation cooling system was applied to reduce the surface temperature of the antennae. The ablative zone was nearly 3.5 cm × 3 cm for MWA, with an output of 60–80 Watt/6–8 min.[18],[19]

Local anesthesia (lidocaine) and preemptive analgesia (morphine) were administrated. Preoperative localization was confirmed with CT images, and the patient was placed in appropriate positions. Once satisfactory anesthesia was achieved, the skin at the puncture point was cut, the ablation microwave antennae were inserted through the deeper layers of tissue to the GGO lesion. This procedure was performed per the preoperative-planned route, and the puncture depth was the preoperative-planned “target skin distance.” MWA was started followed by the connection of cold circulating pipes and pumps to the MWA antennae and machine. The technical success was that the “postablation GGO” was generally 0.5–1.0 cm larger than the tumor sites. After the procedure, the MWA antennae were withdrawn, local disinfection was performed, and a bandage was applied to protect the wound.

Follow-up imaging and outcome assessment

A non-contrast chest CT scan was conducted on all the patients, 24–48 h after MWA, for detecting the potential complications and the technique effectiveness. Then, a serial of repeated contrast-enhanced CT (CECT) scans was conducted on the patients at 1-, 3-, 6-, 9-, and 12-month intervals. Thereafter, follow-up visits were conducted every 6 months.

Evaluation of local response and survival

The response was determined 4–6 weeks after ablation of the lesion and then compared with the baseline: (1) complete ablation, with any one of the following patterns: (a) lesion disappeared; (b) cavity completely formed; (c) fibrosis or scar; (d) solid nodule involution or no change, without contrast enhanced signs on the CT; (e) atelectasis, lesion in atelectasis without contrast enhanced signs on the CT; (2) local progression, with any one of the following patterns: (a) cavity partially formed, with some remaining solid parts or liquid components, and with irregular peripheral or internal enhancement signs on the CT; (b) partial fibrosis, with solid residues in the fibrotic lesion, presented as irregular peripheral or internal enhancement signs on CT; (c) solid nodules with increased size, which also presented as irregular peripheral or internal enhancement signs on CT; (d) atelectasis, lesion in atelectasis with contrast enhanced signs on the CT; (e) enlarging or new GGO or nodule on CT images around the ablated lesion.

When the inclusion criteria for MWA were met, the local tumor progression was treated again by MWA. Tumor recurrence other than local tumor progression was defined as distant metastasis. With the results of follow-up, 3 years local progression-free survival (LPFS), 3 years cancer-specific survival (CSS), and 3 years overall survival (OS) were assessed. LPFS was defined as the time between the initial ablation and the first radiologic evidence of local progression. CSS was defined as the time between the initial ablation and 3 years cancer-related death. The 3 years OS was defined as the time between the initial ablation and death from any cause.

Complication assessment

The complications were assessed according to the classifications of the American Society of Interventional Radiology (SIR) criteria.[27] The definition of major complication was an event that leads to substantial morbidity and disability (e.g., unexpected loss of an organ) increasing the level of care, hospital admission, or substantially lengthened hospital stay (SIR classifications C-E). This also included any case in which the blood transfusion or interventional drainage procedure was required. Any patient death within 30 days after image-guided tumor ablation should be addressed (SIR classification F). All other events were considered as minor complications. According to the time of occurrence, the complications were classified into: immediate complications (<24 h after ablation), perioperative complications (24 h–30 d after ablation), and delayed complications (>30 d after ablation).

Statistical analysis

Data analysis was performed with SPSS for Windows Version 13.0 (IBM, Chicago, IL). OS curves were constructed with the Kaplan–Meier method and compared with the log-rank test. Comparison between groups was performed with Chi-square test. Statistical significance was set at P < 0.05.


 > Results Top


Clinical outcomes

Ablation procedure was completed based on the planned protocol and well-tolerated in all sessions. The technical success rate was 100% in 51 sessions. A total of 51 lesion sites were entirely covered by the ablative zones 24–48 h after initial MWA. The technique effectiveness rate was 100%.

By the time of 31 March 2018, no patients were lost to follow-up, and the median follow-up period after ablation was (27.02, range: 7–45 months) with CECT [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]. One patient (2%, 1/51) showed local tumor progression 14 months after MWA. Therefore, a second MWA was performed on this patient. This tumor presented complete ablation after the second MWA. The patient died due to liver cirrhosis 15 months after the second MWA. At the 1-year follow-up, 51 ablated tumors (51 MWA sessions) were controlled in all 51 patients. At the 2-year follow-up, 50 ablated tumors (51 MWA sessions) were controlled in 50 patients, and one patient died. At the 3-year follow-up, 49 ablated tumors (49 MWA sessions) were controlled in 49 patients. The 1-year, 2-year, and 3-year local control rates were 100%, 98%, and 100%, respectively.
Figure 1: Female: 78-year-old patient with 28 mm × 22 mm right lung part-solid ground-glass opacity (invasive adenocarcinoma) complete ablation. (a) Ground-glass opacity lesion (1 mm, arrow) seen on computed tomography before microwave ablation. (b) The microwave antenna was punctured into lesion (arrow). (c) Ablated lesion computed tomography scan immediately postmicrowave ablation. (d) Follow-up computed tomography scan at 6 months shows a fibrous scar at the site of the ablated lesion (arrow). (e) 12 months after ablation, ablated lesion (arrow) significantly involution. (f) 42 months after ablation, lesion become fiber cord (arrow)

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Figure 2: Female: 68-year-old patient with 12 mm × 10 mm right lung pure ground-glass opacity (minimally invasive adenocarcinoma) complete ablation. (a) Ground-glass opacity lesion (1 mm, arrow) seen on computed tomography before microwave ablation. (b) The microwave antenna was punctured into lesion (arrow). (c) Ablated lesion computed tomography scan immediately postmicrowave ablation. (d) 3 months after ablation, the ablated lesion shows a fibrous hyperplasia (arrow). (e) 12 months after ablation, fibrous hyperplasia of ablated lesion (arrow) involution. (f) 36 months after ablation, lesion become fiber scar (arrow)

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Figure 3: Male: 62-year-old patient with 29 mm × 20 mm right lung pure ground-glass opacity (invasive adenocarcinoma) complete ablation. (a) Ground-glass opacity lesion (1 mm, arrow) seen on computed tomography before microwave ablation. (b) The microwave antenna was punctured into lesion (arrow). (c) Ablated lesion computed tomography scan immediately postmicrowave ablation. (d) 6 months after ablation, the ablated lesion shows a fibrous hyperplasia (arrow). (e) 12 months after ablation, fibrous hyperplasia of ablated lesion (arrow) involution. (f) 40 months after ablation, lesion become fiber cord (arrow)

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Figure 4: Female: 52-year-old patient with 23 mm × 22 mm right lung pure ground-glass opacity (invasive adenocarcinoma) complete ablation. (a) Ground-glass opacity lesion (1 mm, arrow) seen on computed tomography before microwave ablation. (b) The microwave antenna was punctured into lesion (arrow). (c) Ablated lesion computed tomography scan immediately postmicrowave ablation. (d) 6 months after ablation, the ablated lesion shows a fibrous hyperplasia (arrow). (e) 36 months after ablation, lesion become fiber cord (arrow)

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Figure 5: Local progression-free survival, cancer-specific OS and OS of all patients

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During the follow-up, two patients died. One died of cerebral infarction 13 months after MWA, and the other patient died of liver cirrhosis 29 months after lung MWA. The recurrence of lung cancer was not observed in neither of the two patients. The 1-year and 3-year LPFS rates were 100% and 98% (50/51) (95% confidence interval [CI], 77.5%–99.5%), respectively. The 1-year and 3-year CSS rates were 100% and 100%, respectively. The 1-year and 3-year OS rates were 100% and 96% (49/51) (95% CI, 77.5%–99.5%), respectively [Figure 5]. No mediastinal lymph node and distant metastasis were observed in all 51 patients.

Side effects and complications

No death-related to the MWA procedure was observed during the procedure or within 30 days after MWA.

Side effects were summarized as follows: (1) Pain – during the procedure, pain was the common side effect under the local anesthesia conditions during the procedure. In 52 sessions of MWA, the patients in eight sessions reported moderate-to-severe pain, of which two sessions were severe. The procedure was stopped when there was severe pain, and it was followed by subcutaneous injection of morphine. At the same time, an adequate amount of sedatives such as midazolam were intravenously administrated. After the procedure of MWA, nine patients suffered from moderate pain, without severe postablation pain. (2) Cough – in 52 sessions of MWA, the patients in seven sessions suffered from moderate-to-severe cough, of which two sessions were severe. The procedure was stopped with severe cough, and it was followed by subcutaneous injection of midazolam, or the procedure would be intermitted. (3) Postablation syndrome – the main symptoms were fever (lower than 38.5°C), fatigue, general malaise, nausea and vomiting, etc., A total of 13 patients showed above postablation syndrome.

Complications were also summarized. Pneumothorax was the most common complication. There was a total of 25 (48.1%, 25/52) cases of pneumothorax, of which five sessions (9.8%) required a chest tube drainage. Hemoptysis was observed in 14 sessions (28.8%, 14/52) and could be effectively relieved with the conventional application of hemostatic agents. In all 14 sessions with hemoptysis, four sessions occurred during the procedure of ablation. The reason was that ablation itself could result in blood coagulation, thus hemoptysis during ablation would be gradually stopped without the need of special treatment). There were 12 sessions (23.1%, 12/52) of pleural effusion, of which three sessions (5.7%) underwent chest tube insertion. About four sessions (7.7%, 4/52) suffered from pneumonia after the procedure, which could be effectively controlled by antibiotics based on the results of the sputum or blood culture. The grade of complications was illustrated [Table 2].
Table 2: Grade of Complications during and postmicrowave ablation (42 sessions)

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 > Discussion Top


Recently, there were a few clinical studies on the outcome and safety of radiofrequency ablation (RFA) in the treatment of GGO–lung cancer.[28],[29] Kodama. et al.[28] reported that lung RFA was performed on 33 patients with 42 lung tumors with ≥50% GGO components. All patients were alive and only one died of brain hemorrhage. OS and CSS rates were 100% and 100% at 1-year, 96.4% and 100% at 3-years, and 96.4% and 100% at 5-years, respectively. Iguchi et al.[29] reported that 16 patients with 17 lung cancer lesions showing GGO received a total of 20 percutaneous CT-guided RFA sessions. The median follow-up period of all the patients was 65.6 months. About 15 patients were alive, while only one patient died of recurrence of other cancer 11.7 months after RFA. OS and disease-specific survival rates were 93.3% and 100% at 1-year, 93.3% and 100% at 5-years, respectively. These results suggested that lung RFA was safe and effective for treating lung cancer with GGO, bringing about promising survival rates. However, there was very few clinical study on the effect and safety of MWA for treating lung cancer with GGO.

MWA has several advantages over RFA, including faster ablations (shorter procedure time), higher temperatures without the limitations related to electric impedance, less sensitivity to tissue type, more consistent results, and less “heat sink” effect for better treating perivascular tissues. In addition, the size of ablation zone could be maximized by simultaneously positioning multiple MWA antennae into the larger lesion.[30],[31],[32],[33],[34],[35],[36],[37] To the best of our knowledge, this study was the first retrospective, multicenter study that aimed to assess the safety, outcomes, and complications of MWA as an alternative approach for treating GGO–lung adenocarcinoma.

In this study, local tumor progression after MWA procedure was 2% (1/51) for the treatment of GGO–lung adenocarcinoma. The incidence of local tumor progression was significantly lower than that of reported in our previous study (23.1%) for treating inoperable stage I solid lung tumors.[18],[19] No mediastinal lymph node and distant metastasis were found in all the 51 patients. The slow-growing nature of GGO–lung adenocarcinoma seemed to contribute to this difference.[38] In addition, GGO-dominant lung adenocarcinoma rarely showed pathologic invasiveness, including lymphatic, vascular, pleural invasion, or lymph node metastasis.[39] The local tumor progression rate may be underestimated; however, it was difficult to differentiate the ablation zone with the tumor margin.[28] Long-term follow-up of the ablated tumors was necessary.

From the follow-up results of this study, the 1-year and 3-year LPFS rates were 100% and 98% (50/51) (95% CI, 77.5%–99.5%), respectively. The 1-year and 3-year CSS rates were 100% and 100%, respectively. The 1-year and 3-year OS rates were 100% and 96% (49/51) (95% CI, 77.5%–99.5%), respectively. These results suggested that MWA was effective in improving the survival of patients with GGO–lung adenocarcinoma.

Pneumothorax was one of the most common complications for MWA. The incidence of pneumothorax in this study was 45.2% (19/42). The incidence of pneumothorax was similar to that of in our previous report.[40],[41],[42] Although the occurrence rate of pneumothorax was high, chest tube insertion was required in only five cases. Other complications consisted of hemoptysis 26.2% (11/42), pleural effusion 33.3% (14/42), pulmonary infection (9.5%, 4/42), severe pain (4.8%, 2/42), severe cough (4.8%, 2/42), and postablation syndromes (31%, 17/42). All these side effects and complications mentioned above could be well controlled through observation or proper treatments. There was no death within 30-day postprocedure in our patient series. Furthermore, ablation procedure was completed per planned protocol and well tolerated in all sessions. The technical success rate was 100% in 52 sessions. This study suggested that MWA was feasible and safe for treating a patient with GGO–lung adenocarcinoma. Since 42 medically inoperable patients were included due to elderly, severe cardiopulmonary dysfunction and other concomitant diseases in this study, we suggested that the application of MWA was for more suitable for medically inoperable patients with GGO–lung adenocarcinoma.

Certainly, there were some limitations in this study. The main limitations were its retrospective nature, relatively short follow-up duration after addressing GGO lesions, as well as the small sample size. Furthermore, this study was not designed to compare the MWA with other treatments such as surgery, stereotactic body radiotherapy, or other local ablation technologies. Prospective multicenter study of MWA with larger sample size would be necessary to better clarify the effectiveness and safety of this treatment strategy.


 > Conclusions Top


CT-guided percutaneous MWA was a feasible, safe, and useful therapeutic approach for GGO–lung adenocarcinoma. It would become an alternative approach for treating medically inoperable patients with peripheral GGO–lung adenocarcinoma.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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