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ORIGINAL ARTICLE
Year : 2019  |  Volume : 15  |  Issue : 4  |  Page : 755-759

Diagnostic ability of percutaneous core biopsy immediately after microwave ablation for lung ground-glass opacity


1 Department of Oncology, Shandong Provincial Hospital Affiliated to Shandong University, Jinan, Shandong Province, China
2 Department of Oncology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong Province, China
3 Department of Oncology, Dongchangfu District People's Hospital Affiliated to Shandong First Medical University, Liaocheng, China

Date of Web Publication14-Aug-2019

Correspondence Address:
Xin Ye
Department of Oncology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, 324 Jingwuweiqi Road, Jinan, Shandong Province 250021
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_399_19

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 > Abstract 


Objectives: The objective of this study is to determine the diagnostic ability of percutaneous core biopsy immediately after microwave ablation (MWA) for lung ground-glass opacity (GGO).
Materials and Methods: Seventy-four patients with 74 lung GGOs were enrolled and treated with MWA. A percutaneous core needle biopsy was performed pre- and immediately post-MWA. All biopsy specimens were histologically examined by hematoxylin and eosin staining and immunostaining. Histologically, atypical adenomatous hyperplasia (AAH), adenocarcinoma in situ (AIS), minimally invasive adenocarcinoma (MIA), and invasive adenocarcinoma (AC) were identified as positive, while chronic inflammation or normal lung tissue was identified as negative.
Results: The outcomes of pre-MWA histological diagnosis were AAH (n = 4), AIS (n = 16), MIA (n = 14), AC (n = 29), chronic inflammation (n = 2), and lung tissue (n = 9) with an 85.1% (63/74) positive diagnosis rate. The outcomes of the immediately post-MWA histological diagnosis were AAH (n = 5), AIS (n = 10), MIA (n = 11), AC (n = 29), chronic inflammation (n = 1), and lung tissue (n = 18) with a 74.3% (55/74) positive diagnosis rate. There was no significant difference in the positive diagnosis rate between the pre- and immediately post-MWA groups (P = 0.10). The outcomes of the combined diagnosis of pre- and immediately post-MWA were AAH (n = 4), AIS (n = 16), MIA (n = 16), AC (n = 31), chronic inflammation (n = 2), and lung tissue (n = 5) with a positive diagnosis rate of 90.5% (67/74), which was higher than that by pre-MWA biopsy (P < 0.05). The main complications were pneumothorax (n = 45, 60.8%), hemoptysis (n = 24, 32.4%), pleural effusion (n = 39, 52.7%), and pulmonary infection (n = 10, 13.5%).
Conclusions: Immediately post-MWA core biopsy has promising efficacy for histological diagnosis of lung GGOs.

Keywords: Biopsy, ground-glass opacity, lung, microwave ablation


How to cite this article:
Wang J, Ni Y, Yang X, Huang G, Wei Z, Li W, Han X, Meng M, Ye X, Lei J. Diagnostic ability of percutaneous core biopsy immediately after microwave ablation for lung ground-glass opacity. J Can Res Ther 2019;15:755-9

How to cite this URL:
Wang J, Ni Y, Yang X, Huang G, Wei Z, Li W, Han X, Meng M, Ye X, Lei J. Diagnostic ability of percutaneous core biopsy immediately after microwave ablation for lung ground-glass opacity. J Can Res Ther [serial online] 2019 [cited 2019 Sep 22];15:755-9. Available from: http://www.cancerjournal.net/text.asp?2019/15/4/755/264288




 > Introduction Top


Ground-glass opacity (GGO) is defined as increased hazy attenuation within a lung that is not associated with obscured underlying vessels. Based on the quantity and scope, GGOs can be divided into focal and diffusive types. In this study, we assess focal GGOs. Pulmonary GGOs are highly associated with lung malignancies.[1] With the widespread use of CT screening, detection of pulmonary GGOs has become increasingly common.

According to the new classification of the International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society in 2011, lung adenocarcinomas (ACs) were classified as atypical adenomatous hyperplasia (AAH), AC in situ (AIS), minimally invasive adenocarcinoma (MIA), and invasive AC having lepidic, acinar, papillary, micropapillary, or solid growth patterns. Sublobar resection is currently advocated for AIS and MIA, while lobectomy with lymph node dissection remains as the standard treatment for invasive AC. However, some GGO patients are not candidates for surgery due to severe medical comorbidities primarily based on poor cardiopulmonary function. For these patients, local thermal ablation mainly including radiofrequency ablation (RFA) or microwave ablation (MWA) is considered as an effective alternative treatment strategy.[2],[3],[4],[5],[6] Recently, we reported our preliminary results and showed promising efficacy and safety of MWA for the treatment of lung GGO AC.[7] However, in cases with a high suspicion of malignant GGOs, biopsy before MWA in a separate session may potentially induce hemorrhage, pneumothorax, pulmonary infection, gas embolism, and cancer seeding along the biopsy puncture tract.[8],[9] In addition, lung biopsy performed immediately before MWA during the same procedure increases the potential difficulties in tumor targeting due to postbiopsy alterations on imaging along with hemorrhage which may blur the tumor and alter the accuracy of MWA antenna placement. Furthermore, biopsy-induced pneumothorax can render the puncture more difficult.

Some clinical studies have reported that cell apoptosis or necrosis gradually progressed after hyperthermia treatment. The morphological features of the tumor cells were preserved for at least 1 month after thermal ablation.[10],[11] Recently, we clarified that post-MWA immediately after a biopsy can distinguish cancer cells or histological types in most cases of lung cancers.[12] However, there are few reports that assessed the diagnostic ability of needle biopsy immediately post MWA for lung GGOs. The purpose of this study was to explore the diagnostic ability of post-MWA core biopsy for GGOs.


 > Materials and Methods Top


Patients

Patients with pure GGO or GGO-dominant lesions (GGO component ≥75%) based on computer tomography (CT) screening were enrolled. The inclusion criteria were as follows: (1) Eastern Cooperative Oncology Group performance status of 0–1; (2) poor cardiopulmonary function for surgery or refuse surgery, (3) biopsies performed pre- and immediately post-MWA; (4) enhanced CT, positron emission tomography-CT, and enhanced magnetic resonance imaging were performed to exclude lymph node metastasis and distance metastasis; and (5) normal hepatic and renal functions.

Steps of biopsy and microwave ablation procedures

  1. The patients were placed in prone, supine, or lateral positions, whichever provided access to the best puncture pathway
  2. All procedures were performed under local anesthesia and CT (Neusoft CT, Neusoft Group Co., Ltd, China) guidance
  3. The ablation antenna was inserted into the lesion
  4. A 16G sleeve-core needle (PRECISA fine-core needle, H. S. Hospital Service S. P. A, Aprilia, Italy) was pierced through the proximal edge of the lesion. The core was then pulled out, with an 18G biopsy needle pierced into the lesion through the 16G sleeve. The strips of specimens, each measuring 1–2 cm, were obtained and preserved in 10% formalin for pathological examination
  5. MWA was performed as described in our previous studies [7],[12]
  6. After MWA, the core of the 16G needle was pulled out with another 18G biopsy needle pierced into the lesion through the 16G sleeve. The strips of specimens were obtained and preserved in another sample bottle containing 10% formalin for pathological examination
  7. The biopsy 16G sleeve-core needle and the ablation antenna were pulled out. The patients underwent thoracic CT scan examination immediately and at 24 h postprocedure.


Pathological examination

In this study, the pathological findings of GGOs at preablation were AAH, AIS, MIA, AC, chronic inflammation, and lung tissue. The pathological findings at postablation were the related histological outcomes accompanied by physical damage or deformation from the burn. AAH, AIS, MIA, and AC were assigned into the positive group, while normal lung tissues and chronic inflammation were allocated into the negative group.

Complications

Treatment-related complications were defined as symptoms that occurred within 30 days of ablation. The severity of the complications was defined in accordance with the Society of Interventional Radiology Standards of Practice Committee classification of complications.[13]

Statistical analysis

Statistical analyses were performed by Pearson's χ2 test. To compare the positive rate of pathological findings of biopsy at pre- and postablation, we used the Pearson's χ2 test. SPSS 17.0 (IBM, Chicago, USA) was used for analyses, and P < 0.05 was considered statistically significant.


 > Results Top


Baseline characteristics

From December 2016 to April 2019, 74 patients with 74 GGOs were enrolled based on the inclusion criteria. The baseline characteristics are shown in [Table 1]. Among these 74 patients, 36 (48.6%) were male and 38 were >60 years. Twenty-seven lesions (36.5%) were located in the upper lobe of the right lung, and the mean long diameter was 17.1 mm. The number of pure GGO and GGO-dominant lesions was 55 (74.3%), and 19 (25.7%), respectively. The mean power of MWA was 57.6 W, and the mean ablation time was 6.9 min. After the procedure, the patients were required to stay in the hospital for at least 24 h. The mean hospitalization period was 3.4 days.
Table 1: Baseline characteristics of the enrolled patients and lung ground-glass opacity

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Pathological findings

The outcomes of pre- and post-MWA pathological findings and final pathological findings are shown in [Table 2] and [Table 3], respectively. The outcomes of pre-MWA histological diagnosis were AAH (n = 4), AIS (n = 16), MIA (n = 14), AC (n = 29), chronic inflammation (n = 2), and lung tissue (n = 9) with a positive diagnosis rate of 85.1% (63/74). The outcomes of immediately post-MWA histological diagnosis were AAH (n = 5), AIS (n = 10), MIA (n = 11), AC (n = 29), chronic inflammation (n = 1), and lung tissue (n = 18) with a positive diagnosis rate of 74.3% (55/74). There was no significant difference in the positive diagnosis rate between the pre- and immediately post-MWA groups (Pearson's χ2 test, P = 0.10).
Table 2: Pathological findings in pre. and postmicrowave ablation biopsies

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Table 3: Pathological findings in the premicrowave ablation biopsies and the final pathological findings

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The combined pre- and immediately post-MWA pathological diagnosis has been termed as the final pathologic diagnosis. This diagnosis is a summary of the pre- and postablation pathological results and the patient's imaging results. The outcomes of the final pathologic diagnosis were AAH (n = 4), AIS (n = 16), MIA (n = 16), AC (n = 31), chronic inflammation (n = 2), and lung tissue (n = 5) with a positive diagnosis rate of 90.5% (67/74), which was higher than diagnosis by pre-MWA biopsy. The mean positive rate of final pathological diagnosis was higher than that of pre-MWA pathological diagnosis.

Four patients were diagnosed as MIA (n = 2) or AC (n = 2) by immediately post-MWA biopsy and as lung tissue by pre-MWA biopsy, suggesting that post-MWA biopsy played an important supplementary role in the final pathologic diagnosis. In two cases, the pathological outcomes before ablation were MIA (n = 1) and AC (n = 1), while the pathological finding at post-MWA was AAH in both the cases.

Adverse effects and complications

The mortality rate related to the procedure was nil during and within 30 days of the procedure. Complications such as pneumothorax in patients in whom the thoracic cavity was closed followed by drainage occurred in 11 sessions (14.9%) after 74 procedures [Table 4]. The other 34 sessions (45.9%) reported mild pneumothorax without the requirement of any treatment. Mild ipsilateral pleural effusion was observed in 39 sessions (52.7%). Mild contralateral pleural effusion occurred in 11 sessions (14.9%) following ipsilateral pleural effusion. Hemoptysis was complained by 24 patients (32.4%), while pulmonary infection was observed in 10 cases (13.5%). The other complications with low incidence included subcutaneous emphysema (n = 3, 4.1%) and mediastinal emphysema (n = 2, 2.7%), which returned to normal after observation. Except for drainage for pneumothorax, the other symptoms were resolved after conservative treatment.
Table 4: Adverse effects and complications

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 > Discussion Top


Differentiation of malignant GGO lesions by CT alone is generally considered to be difficult despite some studies showing positive results.[14],[15],[16] Percutaneous CT-guided core biopsy is an accurate diagnostic technique for lung lesions with a diagnostic accuracy of up to 90%.[17],[18],[19] For GGO lesions, a biopsy is more likely to be affected by hemorrhage during the procedure. Hemorrhage can mask GGO lesions leading to a relative lower diagnostic accuracy than that of solid nodules. Chang et al. reported a CT-guided needle cutting biopsy-positive ratio (malignant and suspicious malignant diagnosis) of 73.7%, while the final diagnostic accuracy validated by surgical pathological findings was 93.4%.[19] Our results indicated an overall (pre- and immediately postablation combination) biopsy-positive rate of 90.5%, which was significantly higher than that in the previously reported literature. This is considered to be related to the following factors. First, we used a coaxial needle biopsy method which obtained more tissue specimens for histological examination. Second, we enrolled part-solid GGOs that were more malignant than pure GGOs, which might increase the positive rate of biopsy to some extent. Most importantly, we performed pre- and immediately postablation core biopsy during the same procedure. Some preclinical and clinical data suggest that the morphological features of tumor cells are preserved after thermal ablation, at least during the 1st month.[10],[20] Tselikas et al. reported a diagnosis of malignancy in 90% of cases who underwent immediately biopsy after lung RFA.[11] Recently, our results also showed that immediately biopsy post-MWA can distinguish cancer cells or histological types in most nonsmall cell lung cancer cases (up to 85.3%).[12]

In this study, our results showed that the positive ratio of pre- and immediately post-MWA biopsy was 85.1 and 74.3%, respectively. In addition, the characteristics of vital tumor tissue were preserved in the immediately post-MWA biopsy samples. Four patients were diagnosed as having MIA (n = 2) or AC (n = 2) by immediately post-MWA biopsy and as having normal lung tissue by pre-MWA biopsy. The positive rate of combined diagnosis in the pre- and the immediately post-MWA group was significantly higher than that in the pre-MWA alone group, indicating that immediately post-MWA biopsy may improve the diagnostic accuracy after GGO ablation treatment.

No periprocedural mortality was observed in the present study. A biopsy performed immediately before MWA is considered to carry a risk of bleeding or pneumothorax which may make it difficult to perform sufficient ablation, especially for lung GGOs.[11] Hence, in this study, we placed the MWA antenna first, and when the position was secured, the biopsy was performed through a second puncture. Although two needle punctures were likely to increase the risk of complications including pneumothorax and bleeding, the major complication was pneumothorax requiring drainage tube placement (14.9%). This result is comparable to that of previous reports.[21],[22],[23] Complications were mainly minor in our study, with mild pneumothorax (45.9%) and mild ipsilateral pleural effusion (52.7%), which recovered after discharge without any intervention. Hemoptysis occurred in 32.4% of the patients, while most of them were mild. MWA may also reduce the risk of bleeding after the biopsy. Therefore, complications of core needle biopsy in combination with MWA in a single session were mild and tolerable.

The main limitation of this technique is that the biopsy results obtained could not be correlated with the resected surgical pathological findings to calculate the sensitivity and specificity. Hence, we suggest all patients undergoing long-term clinical and imaging follow-up even with the absence of histologically diagnosed malignancy. Second, our results are based on the experience at a single center. Prospective multicenter study of CT-guided needle biopsy and MWA with larger sample size would be necessary to better clarify the effectiveness and safety of this strategy.


 > Conclusions Top


Immediately post-MWA core biopsy has promising efficacy for histological diagnosis of lung GGOs. Combination of pre- and immediately post-MWA core biopsy in a single session can improve the diagnostic ability for GGOs.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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Duann CW, Hung JJ, Hsu PK, Huang CS, Hsieh CC, Hsu HS, et al. Surgical outcomes in lung cancer presenting as ground-glass opacities of 3 cm or less: A review of 5 years' experience. J Chin Med Assoc 2013;76:693-7.  Back to cited text no. 1
    
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Kodama H, Yamakado K, Hasegawa T, Takao M, Taguchi O, Fukai I, et al. Radiofrequency ablation for ground-glass opacity-dominant lung adenocarcinoma. J Vasc Interv Radiol 2014;25:333-9.  Back to cited text no. 2
    
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Iguchi T, Hiraki T, Gobara H, Fujiwara H, Matsui Y, Soh J, et al. Percutaneous radiofrequency ablation of lung cancer presenting as ground-glass opacity. Cardiovasc Intervent Radiol 2015;38:409-15.  Back to cited text no. 3
    
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Yang X, Ye X, Lin Z, Jin Y, Zhang K, Dong Y, et al. Computed tomography-guided percutaneous microwave ablation for treatment of peripheral ground-glass opacity-lung adenocarcinoma: A pilot study. J Cancer Res Ther 2018;14:764-71.  Back to cited text no. 7
    
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Hiraki T, Mimura H, Gobara H, Sano Y, Fujiwara H, Iguchi T, et al. Two cases of needle-tract seeding after percutaneous radiofrequency ablation for lung cancer. J Vasc Interv Radiol 2009;20:415-8.  Back to cited text no. 8
    
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Yamakado K, Akeboshi M, Nakatsuka A, Takaki H, Takao M, Kobayashi H, et al. Tumor seeding following lung radiofrequency ablation: A case report. Cardiovasc Intervent Radiol 2005;28:530-2.  Back to cited text no. 9
    
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Tselikas L, de Baere T, Deschamps F, Hakimé A, Besse B, Teriitehau C, et al. Diagnostic yield of a biopsy performed immediately after lung radiofrequency ablation. Eur Radiol 2017;27:1211-7.  Back to cited text no. 11
    
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Wei Z, Wang Q, Ye X, Yang X, Huang G, Li W, et al. Microwave ablation followed by immediate biopsy in the treatment of non-small cell lung cancer. Int J Hyperthermia 2018;35:262-8.  Back to cited text no. 12
    
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Kim HY, Shim YM, Lee KS, Han J, Yi CA, Kim YK. Persistent pulmonary nodular ground-glass opacity at thin-section CT: Histopathologic comparisons. Radiology 2007;245:267-75.  Back to cited text no. 14
    
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Mukherjee S, Bandyopadhyay G, Bhattacharya A, Ghosh R, Barui G, Karmakar R. Computed tomography-guided fine needle aspiration cytology of solitary pulmonary nodules suspected to be bronchogenic carcinoma: Experience of a general hospital. J Cytol 2010;27:8-11.  Back to cited text no. 17
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Ohno Y, Hatabu H, Takenaka D, Higashino T, Watanabe H, Ohbayashi C, et al. CT-guided transthoracic needle aspiration biopsy of small (≤20 mm) solitary pulmonary nodules. AJR Am J Roentgenol 2003;180:1665-9.  Back to cited text no. 23
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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