Risk of Pleural Recurrence After Computed Tomographic-Guided Percutaneous Needle Biopsy in Stage I Lung Cancer Patients

Transcription

1 GENERAL THORACIC Risk of Pleural Recurrence After Computed Tomographic-Guided Percutaneous Needle Biopsy in Stage I Lung Cancer Patients Masayoshi Inoue, MD, PhD, Osamu Honda, MD, PhD, Noriyuki Tomiyama, MD, PhD, Masato Minami, MD, PhD, Noriyoshi Sawabata, MD, PhD, Yoshihisa Kadota, MD, PhD, Yasushi Shintani, MD, PhD, Yuko Ohno, PhD, and Meinoshin Okumura, MD, PhD Department of General Thoracic Surgery, Diagnostic and Interventional Radiology, and Department of Mathematical Health Science, School of Health Science, Osaka University Graduate School of Medicine, Osaka, Japan Background. A computed tomographic-guided percutaneous needle biopsy () is useful as an option for pathologic diagnosis of lung cancer, especially in patients with peripheral small-sized nodules. We aimed to assess the risk of pleural seeding of cancer cells, leading to postoperative relapse with dissemination caused by the procedure. Methods. We investigated the clinical outcomes of 447 stage I lung cancer patients. Survival analysis was performed using the Kaplan-Meier method and a log-rank test. Pleural recurrence rates were also determined. Furthermore, propensity score matching analysis was used to reduce background bias from patient characteristics. Results. The 5-year, disease-free survival rate was 89.1% in patients diagnosed with, and 85.5% in those diagnosed using a transbronchial biopsy or open lung biopsy procedure. Local recurrence with pleural dissemination was found in 8 of 13 recurrence cases (61.5%) in the group, which was higher as compared with the transbronchial biopsy or open lung biopsy group (p < 0.01). Subset analyses of p stage IB cases and those with subpleural lesions showed that local recurrence with dissemination was significantly more frequent in the group (p 0.02 and p < 0.01, respectively). In patients with subpleural lesions diagnosed with, the rate of local recurrence with dissemination was 15.4%. Propensity score matching analysis confirmed the significantly increased frequency of pleural dissemination after. Conclusions. The procedure might increase the risk of pleural implantation in stage I lung cancer patients, especially p stage IB cases with subpleural lesions, whereas the overall disease-free survival rate was not affected by this small population of patients with recurrence. (Ann Thorac Surg 2011;91: ) 2011 by The Society of Thoracic Surgeons The standard diagnostic modality for lung cancer is a transbronchial biopsy (TBB) procedure using fiberoptic bronchoscopy with fluoroscopic imaging. The TBB is not indicated for peripheral small-sized nodules or ground glass opacity, which cannot be detected fluoroscopically; thus, a computed tomographic (CT)-guided or ultrasound-guided percutaneous core needle biopsy is occasionally used. Otherwise, histologic diagnosis is obtained by partial resection of the lung or a needle biopsy performed during surgery. A CT-guided percutaneous core needle biopsy () is a useful procedure to accurately approach lesions that cannot be visualized by TBB, even for smallsized nodules [1, 2]. Bronchiolo-alveolar adenocarcinoma showing ground glass opacity can also be diagnosed by [3]. However, several complications associated with have been reported. For example, pneumothorax and intrapulmonary hemorrhage occurred in 23% to Accepted for publication Dec 16, Address correspondence to Dr Inoue, Department of General Thoracic Surgery, Osaka University Graduate School of Medicine, L5-2-2 Yamadaoka, Suita-city, Osaka , Japan; mi@thoracic.med.osakau.ac.jp. 55%, and 4%, respectively, of all patients examined [4 6]. There are also several case reports of an air embolism causing a brain or cardiac infarction, which is extremely rare but sometimes fatal [7 10]. In addition, several case reports have noted cancer cell implantation along the biopsy route, and salvage treatment including full-thickness excision of the chest wall [11 15]. However, the risk of pleural seeding associated with remains unclear, because local recurrence with pleural dissemination or malignant effusion is a common relapse pattern and not always caused by a percutaneous core biopsy. Because locally advanced lung cancer often shows frequent recurrence, including pleural dissemination, this study focused on stage I patients with completely resected lung cancer who showed better outcomes with fewer relapses to assess the risk of pleural seeding by. Patients and Methods Patients A review of the records was made of all 447 consecutive patients with p stage I peripheral lung cancer who underwent a complete resection between 1992 and by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur

2 Ann Thorac Surg INOUE ET AL 2011;91: PLEURAL RECURRENCE AFTER PERCUTANEOUS BIOPSY Table 1. Characteristics of 447 Lung Cancer Patients Classified as p Stage I Who Underwent Complete Resection Median age (y) Sex Male Female p Stage IA IB Histology Adenocarcinoma Squamous Others 5 15 Pleural involvement Positive Negative Procedure Pneumonectomy 0 1 Lobectomy Segmentectomy Wedge resection 6 15 computed tomographic-guided percutaneous core needle biopsy; OLB open lung biopsy; squamous squamous cell carcinoma; TBB transbronchial biopsy. at Osaka University Hospital in Osaka, Japan. The institutional review board of Osaka University approved this study and waived the need for patient consent. Patient characteristics including the diagnostic methods used are summarized in Table 1. There were 326 patients with p stage IA and 121 with p stage IB. Adenocarcinoma was the most frequent histology, accounting for 368 cases (82.3%). There was no significant difference between patients who underwent a and those who underwent a TBB or open lung biopsy (OLB) in regard to the clinical factors of age, sex, p stage, histology, pleural factor, and operative procedure. The proportion of ground glass opacity was 33 of 131 (25.2%) in the group and 56 of 316 (17.2%) in the TBB or OLB groups. All patients underwent a pulmonary resection through an open or mini-thoracotomy with video-assisted thoracic surgery. The average postoperative follow-up period was 60.4 months. Diagnostic Method and Indication for In principle, we perform a TBB for pathologic diagnosis of lung cancer, especially for patients with pulmonary lesions that can be recognized on chest roentgenogram. The method is used for cases that have no indication or cannot be diagnosed with TBB. Patients who have visible lesions or who are treated with bronchoplasty were excluded from the present analysis to compare the recurrence patterns between TBB and to reduce selection bias by tumor location. Intraoperative diagnosis with partial resection of the lung or a core needle biopsy during a thoracotomy was performed 1067 when no pathologic diagnosis was obtained before surgery with TBB or. As for the technique used, an 18-gauge cutting needle was guided into the lesion through the intercostal space using CT imaging under infiltration anesthesia, with a duplicate biopsy performed to obtain sufficient material. Fine-needle aspiration cytology was occasionally used in patients who had emphysematous lungs or nonperipheral tumors to avoid complications, such as critical pneumothorax or pulmonary hemorrhage. Patients diagnoses based on intraoperative needle biopsy findings were included in the OLB group. Brain CT or magnetic resonance imaging, abdominal CT, and bone scintigraphy were used to detect distant metastases for clinical staging. At our institution, positron emission tomographic-ct was used instead of bone scintigraphy at the discretion of the physician since Pathologic staging was classified according to the TNM classification, version 7. Survival Analysis With Recurrence Pattern Postoperative survival outcomes, including recurrence patterns were analyzed. Contrast chest CT, contrast brain CT, or magnetic resonance imaging, and bone scintigraphy were routinely performed every year during follow-up examinations, whereas chest roentgenograms and measurements of the serum carcino-embryonic antigen as a tumor marker were performed every 3 to 6 months to survey for recurrence for 5 years after surgery. Subset survival analyses were also performed according to p stage (IA vs IB) and tumor location (subpleural [SPL] vs nonsubpleural [NSPL] sites). A SPL lesion was defined as a tumor seen contacting the visceral pleural in preoperative CT imaging. Recurrence with pleural dissemination was defined as a pleural lesion seen growing on a CT image or malignant pleural effusion proven by cytologic findings from the initial relapse site. Recurrence in a hilar or mediastinal lymph node without dissemination was not considered to be a plural relapse. Positron emission tomographic-ct was used in several recent cases to support the diagnosis. The disease-free survival (DFS) rate was calculated using the Kaplan-Meier method, and the prognostic effects of the tested variables were analyzed using a log-rank test. A 2 test and Fisher s exact test were used to compare ratios between groups. Propensity Score Matching Analysis We performed propensity score-matching analysis to reduce the selection bias for each group (, TBB or OLB). The propensity score for each case was calculated using multi-logistic analysis, with age, sex, tumor diameter, tumor location, operative procedure, and observation period as variables. The case and control patients were selected by matching propensity scores without clinical information regarding outcome. Statistical calculations were performed using the commercially available software program JMP, version 8 (SAS, Cary, NC). GENERAL THORACIC

3 GENERAL THORACIC 1068 INOUE ET AL Ann Thorac Surg PLEURAL RECURRENCE AFTER PERCUTANEOUS BIOPSY 2011;91: Fig 1. Disease-free survival (DFS) rates in p stage I lung cancer patients according to diagnostic method. No significant difference was found between the computed tomographic-guided percutaneous core needle biopsy () and transbronchial biopsy (TBB) or open lung biopsy (OLB) groups. (NS not significant.) Results Disease-Free Survival by Diagnostic Method Diagnostic was performed in 131 patients (29.3%), whereas TBB and OLB were performed in 175 (39.1%) and 141 (31.5%), respectively. The average tumor size was 2.5 cm in the group, whereas the tumor size was 3.1 and 1.8 cm in the TBB and OLB groups, respectively. The difference in tumor diameter might have been caused by the diagnostic procedure indication and therefore it affected patient selection bias. The 5-year DFS rate was 89.1% for the group and 85.5% for the TBB or OLB groups (Fig 1, not significant). In addition, the 5-year DFS rate was 82.0% in patients diagnosed using TBB, which tended to be worse than that for the group (p 0.09). Rate of Local Recurrence With Pleural Dissemination The rate of local recurrence with pleural dissemination was determined based on a diagnostic method. The average postoperative observation period was 66.5 for the group and 57.9 months for the TBB or OLB groups. Pleural recurrence with dissemination was found in 6.1% of all patients in the group, as compared with 1.6% in the TBB or OLB groups (Table 2) (p 0.02). In addition, such a recurrence was observed in 5 of 175 patients (2.9%) in the TBB group, whereas no case of local Table 2. Rate of Local Recurrence With Pleural Dissemination According to Diagnostic Procedure LRPD/all pts 8/131 (6.1%) a 5/316 (1.6%) a LRPD/recurrent pts 8/13 (61.5%) b 5/38 (13.2%) b a p 0.02; b p 0.01 by Fisher s exact test. computed tomographic-guided percutaneous core needle biopsy; LRPD local recurrence with pleural dissemination; OLB open lung biopsy; pts patients; TBB transbronchial biopsy. Table 3. Rates of Local Recurrence With Pleural Dissemination According to p Stage and Tumor Location p Stage IA LRPD/all pts 3/101 (3.0%) 2/225 (0.9%) LRPD/recurrent pts 3/6 (50.0%) 2/21 (9.5%) p Stage IB LRPD/all pts 5/30 (16.7%) a 3/91 (3.3%) a LRPD/recurrent pts 5/7 (71.4%) a 3/17 (17.6%) a SPL LRPD/all pts 8/52 (15.4%) b 2/131 (1.5%) b LRPD/recurrent pts 8/10 (80.0%) b 2/20 (10.0%) b NSPL LRPD/all pts 0/79 (0%) 3/185 (1.6%) LRPD/recurrent pts 0/3 (0%) 3/18 (16.7%) a p 0.02; b p 0.01 by Fisher s exact test. computed tomographic-guided percutaneous core needle biopsy; LRPD local recurrence with pleural dissemination; NSPL nonsubpleural lesion; OLB open lung biopsy; pts patients; SPL subpleural lesion; TBB transbronchial biopsy. recurrence with dissemination was found in the OLB group. When analyzing only recurrent cases, the rate of pleural recurrence was 61.5% for the group, which was significantly higher than that for the TBB or OLB groups (Table 2)(p 0.01). We found no evidence of local relapse at the thoracotomy site or needle track in any of the patients. Subset Analysis According to p Stage and Tumor Location in the Lung Subset analysis by p stage showed that the 5-year DFS rate was 90.4% and 76.5% for p stage IA and IB, respectively (p 0.01). There was no survival difference between the and the TBB or OLB groups for both p stage IA and IB patients. For those classified as p stage IA, the 5-year DFS rate was 93.5% in the group and 88.5% in the TBB or OLB groups. Local recurrence with pleural dissemination was found in 3% of all patients and 50% of patients with recurrence in the group, which was not significantly different from those rates for the TBB or OLB groups (Table 3). On the other hand, the 5-year DFS rate for the p stage IB was 72.6% in the group and 78.2% in the and TBB or OLB groups. The rate of local recurrence with dissemination was 16.7% of all patients (p 0.02) and 71.4% of patients with recurrence (p 0.02) in the group, which were significantly greater than in the TBB or OLB groups (Table 3). Thus, a larger tumor might have a higher potential risk of pleural spreading of cancer cells from the group. Furthermore, because a core needle biopsy procedure for a subpleural lesion (SPL) may cause spreading of cancer cells into the pleural cavity, we evaluated the influence of tumor location by dividing the patients into 2 groups: (1) those with an SPL and (2) those with a nonsubpleural lesion (NSPL). The 5-year DFS rate for those groups was 91.8% and 79.0%, respectively. As

4 Ann Thorac Surg INOUE ET AL 2011;91: PLEURAL RECURRENCE AFTER PERCUTANEOUS BIOPSY shown in Figure 2A, DFS for patients with an SPL was significantly worse than that for those with an NSPL (p 0.01). Although there were 50 patients with a tumor shown by pathologic findings to involve the visceral pleura in the SPL group, there were no significant differences in regard to DFS and pleural recurrence rates between patients classified as p factor ( ) and those as p factor ( ). In addition, a subgroup analysis of patients with an SPL found no survival difference between the and the TBB or OLB groups (Fig 2B). However, the rate of local recurrence with dissemination was significantly higher in the group as compared with the TBB or OLB groups (Table 3). Pleural relapse among patients with recurrence was 80.0% in the group as compared with 10.0% in the TBB group of patients with an SPL. As a result, the local pleural recurrence rate after was 15.4% in patients with Table 4. Characteristics of 254 Patients in the or the TBB or OLB Groups Matched by Propensity Score Median age (years) Sex Male Female Mean tumor diameter (cm) p stage IA IB Histology Adenocarcinoma Squamous Others 5 7 Operative procedure Pneumonectomy/lobectomy Segmentectomy/wedge resection Tumor location SPL NSPL Pleural involvement Positive Negative Mean observation period (mo) GENERAL THORACIC computed tomographic-guided percutaneous core needle biopsy; NSPL nonsubpleural lesion; OLB open lung biopsy; SPL subpleural lesion; squamous squamous cell carcinoma; TBB transbronchial biopsy. an SPL, 10.3% patients in p stage IA, and 21.7% in p stage IB. On the other hand, no pleural recurrence was seen after in patients with an NSPL. Propensity Score Matching Analysis Of the 447 patients, 127 were extracted from the and TBB or OLB groups using propensity score matching to confirm the significant risk of pleural dissemination after. Their background characteristics were matched, as shown in Table 4. The rate of local recurrence with pleural dissemination was observed in 6.3% of all patients in the group, as compared with 0.8% in the TBB or OLB groups (Table 5) (p 0.04). When analyzing only recurrent cases, the rate of pleural relapse reached 61.5% for the group, which was signifi- Table 5. Rate of Local Recurrence With Pleural Dissemination According to Diagnostic Procedure With Propensity Score Matching Analysis Fig 2. Disease-free survival rates (DFS) according to tumor location. (A) Patients with a subpleural (SPL) lesion had a significantly worse outcome than those with a nonspl lesion. (B) DFS rates in patients with a subpleural lesion according to diagnostic method. There was no difference in regard to the diagnosis between the computed tomographic-guided percutaneous core needle biopsy () and transbronchial biopsy (TBB), or open lung biopsy (OLB) groups. (NS not significant.) LRPD/all patients 8/127 (6.3%) a 1/127 (0.8%) a LRPD/recurrent patients 8/13 (61.5%) b 1/16 (6.3%) b a p 0.04; b p 0.01 by Fisher s exact test. computed tomographic-guided percutaneous core needle biopsy; LRPD local recurrence with pleural dissemination; OLB open lung biopsy; TBB transbronchial biopsy.

5 GENERAL THORACIC 1070 INOUE ET AL Ann Thorac Surg PLEURAL RECURRENCE AFTER PERCUTANEOUS BIOPSY 2011;91: Table 6. Rate of Local Recurrence With Pleural Dissemination According to p Stage and Tumor Location With Propensity Score Matching Analysis cantly higher than that for the TBB or OLB groups (Table 5) (p 0.01). In addition, subset analyses for p stage and tumor location in the lung using the propensity score matched groups revealed a higher risk of recurrence with pleural dissemination in patients classified as p stage IB or patients with an SPL (Table 6). Comment p Stage IA LRPD/all pts 3/99 (3.0%) 1/90 (1.1%) LRPD/recurrent pts 3/6 (50.0%) 1/8 (12.5%) p Stage IB LRPD/all pts 5/28 (17.9%) a 0/37 (0%) a LRPD/recurrent pts 5/7 (71.4%) b 0/8 (0%) b SPL LRPD/all pts 8/51 (15.7%) b 0/47 (0%) b LRPD/recurrent pts 8/10 (80.0%) b 0/8 (0%) b NSPL LRPD/all pts 0/76 (0%) 1/80 (1.3%) LRPD/recurrent pts 0/3 (0%) 1/8 (12.5%) a p 0.01; b p 0.01 by 2 test. computed tomographic-guided percutaneous core needle biopsy; LRPD local recurrence with pleural dissemination; NSPL nonsubpleural lesion; OLB open lung biopsy; pts patients; SPL subpleural lesion; TBB transbronchial biopsy. The is a useful diagnostic procedure for patients with peripheral or small-sized pulmonary lesions, because entry of the biopsy needle into the tumor can be accurately visualized with fluoroscopy. The disadvantageous complications related to include pneumothorax, pulmonary hemorrhage, air embolism, and cancer cell seeding, which may be reduced by using fine-needle aspiration with a 21- guage to 23-gauge needle [16, 17]. The possibility of pleural seeding causing pleural dissemination after a percutaneous needle biopsy procedure has been noted, although survival analyses are lacking [18]. Diagnostic imaging techniques have been developed to obtain accurate clinical diagnosis, such as positron emission tomography in addition to conventional or thin-slice CT, whereas percutaneous CT-guided needle biopsy methods have been reported, along with CT fluoroscopy or multi-planar reconstruction imaging techniques [19, 20]. Thus, we reconsidered the efficacy of and the proper indications for its use with lung cancer diagnoses. In the present study, although a high risk of local recurrence with pleural dissemination after was identified, the postoperative DFS rate was similar to that for patients diagnosed with TBB or OLB. A propensity score matching analysis showed a higher risk of pleural seeding after, with p stage IB patients, with an SPL in particular, showing a higher risk of pleural relapse. Therefore, we propose that should be limited to cases that absolutely require a pathologic diagnosis for deciding treatment strategy. Postoperative outcome findings, according to a diagnostic method, revealed a better tendency in the group than in the TBB group in the present study. Because the average tumor size was smaller in the group, it is possible that much earlier diseases were included. A large study of patients extracted from the Surveillance, Epidemiology, and End Results Registry showed no increase in overall or cancer death after a preoperative percutaneous needle biopsy [21]. In addition, we previously reported the characteristics of smallsized lung cancer with clinicopathologic analyses and found excellent postoperative survival [22]. Nevertheless, local recurrence with pleural dissemination was more frequent in the present group, which included a large percentage of patients with smaller lesions. These results suggest that better prognosis due to the major proportion of small-sized early diseases could mask the minor population suffering from local recurrence with pleural dissemination. Thus, except for the evident biopsy route through the chest wall, it might be difficult to recognize the risk of pleural seeding after, which was relatively rare among all cases that underwent resection. In addition, our results showed a higher risk of pleural seeding in the group as compared with the TBB or OLB groups for p stage IB patients, suggesting a relationship between tumor size and pleural dissemination in cases with larger tumors diagnosed with. Because tumors with pleural invasion have the potential to cause pleural dissemination in general, we focused on patients with SPLs in the present study. Visceral pleural invasion is known to be one of the most powerful factors leading to a poor prognosis in patients with completely resected lung cancer [23]. In the new TNM classification (version 7), tumors with visceral pleural invasion are classified as T2. In the present study, the DFS rate was significantly worse in the SPL group, of which one-third of the population had pleural invasion shown in histologic findings. Although was not found to have a negative impact on DFS, local recurrence with pleural dissemination was more frequent as compared with that in patients with an SPL who underwent TBB or OLB. Avoidance of preoperative may contribute to further improvement in the DFS rate for patients with SPLs, because was more often indicated in patients with smaller lesions, probably indicating earlier disease, as compared with the TBB group. On the other hand, there was no pleural relapse in patients with NSPLs after. Together, these results suggest that can be safely recommended with respect to pleural seeding in patients with tumors shown not to have pleural involvement on CT scan images.

6 Ann Thorac Surg INOUE ET AL 2011;91: PLEURAL RECURRENCE AFTER PERCUTANEOUS BIOPSY Based on data obtained from intraoperative lavage cytology findings, it was recently reported that there is little risk of causing pleural dissemination [24]. However, the phenomenon of extrapulmonary seeding by fine-needle aspiration was observed in a clinical investigation using resected lungs [25], as cancer cells were detected in 60% of all cells in pulmonary surface lavage cytology samples after puncture with a 22-gauge needle. In the present study, was performed using an 18-gauge cutting biopsy needle for histologic diagnosis; thus the risk of extrapulmonary seeding might have been higher than that using a fine needle for aspiration cytology. It is also evident that seeded cancer cells cannot always generate pleural dissemination, as it probably requires several factors, such as adhesion, vascular generation, and transformation. When a percutaneous core biopsy is indicated, it is important to consider how to prevent tumor cell seeding. For example, an intentional approach through the pulmonary mesenchyme for an SPL might reduce implantation of cancer cells, because no pleural recurrence was found in the present patients with an NSPL after. We also performed propensity score matching analysis to reduce selection bias according to the oncologic characteristics of the and TBB or OLB groups. This analysis clarified the higher risk of pleural recurrence after, especially in patients with p stage IB and an SPL. In summary, we investigated the risk of pleural dissemination after based on the outcomes of stage I lung cancer patients. The for larger subpleural lesions should be limited to high-risk patients for whom pathologic diagnosis is absolutely necessary to decide treatment strategy. Otherwise, rapid diagnosis with frozen sections obtained during the operation, followed by radical resection, is recommended when preoperative diagnosis cannot be obtained by TBB. References 1. Tomiyama N, Mihara N, Maeda M, et al. CT-guided needle biopsy of small pulmonary nodules: value of respiratory gating. Radiology 2000;217: Ohno Y, Hatabu H, Takenaka D, et al. CT-guided transthoracic needle aspiration biopsy of small ( or 20 mm) solitary pulmonary nodules. AJR Am J Roentgenol 2003;180: Shimizu K, Ikeda N, Tsuboi M, Hirano T, Kato H. Percutaneous CT-guided fine needle aspiration for lung cancer smaller than 2 cm and revealed by ground-glass opacity at CT. Lung Cancer 2006;51: Geraghty PR, Kee ST, McFarlane G, Razavi MK, Sze DY, Dake MD. CT-guided transthoracic needle aspiration biopsy of pulmonary nodules: needle size and pneumothorax rate. Radiology 2003;229: Chakrabarti B, Earis JE, Pandey R, et al. Risk assessment of pneumothorax and pulmonary haemorrhage complicating percutaneous co-axial cutting needle lung biopsy. Respir Med 2009;103: Yeow KM, Su IH, Pan KT, et al. Risk factors of pneumothorax and bleeding: multivariate analysis of 660 CT-guided coaxial cutting needle lung biopsies. Chest 2004;126: Ishikawa Y, Matsuguma H, Nakahara R, Ui A, Suzuki H, Yokoi K. Arterial air embolism: a rare but life-threatening 1071 complication of percutaneous needle biopsy of the lung. Ann Thorac Surg 2009;87: Hiraki T, Fujiwara H, Sakurai J, et al. Nonfatal systemic air embolism complicating percutaneous CT-guided transthoracic needle biopsy: four cases from a single institution. Chest 2007;132: Lattin G Jr, O Brien W Sr, McCrary B, Kearney P, Gover D. Massive systemic air embolism treated with hyperbaric oxygen therapy following CT-guided transthoracic needle biopsy of a pulmonary nodule. J Vasc Interv Radiol 2006;17: Mansour A, Abdel Raouf S, Qandeel M, Swaidan M. Acute coronary artery air embolism following CT-guided lung biopsy. Cardiovasc Intervent Radiol 2005;28: Kim JH, Kim YT, Lim HK, Kim YH, Sung SW. Management for chest wall implantation of non-small cell lung cancer after fine-needle aspiration biopsy. Eur J Cardiothorac Surg 2003;23: Kara M, Alver G, Sak SD, Kavukçu S. Implantation metastasis caused by fine needle aspiration biopsy following curative resection of stage IB non-small cell lung cancer. Eur J Cardiothorac Surg 2001;20: Voravud N, Shin DM, Dekmezian RH, Dimery I, Lee JS, Hong WK. Implantation metastasis of carcinoma after percutaneous fine-needle aspiration biopsy. Chest 1992;102: Redwood N, Beggs D, Morgan WE. Dissemination of tumour cells from fine needle biopsy. Thorax 1989;44: Seyfer AE, Walsh DS, Graeber GM, Nuno IN, Eliasson AH. Chest wall implantation of lung cancer after thin-needle aspiration biopsy. Ann Thorac Surg 1989;48: Tomiyama N, Yasuhara Y, Nakajima Y, et al. CT-guided needle biopsy of lung lesions: a survey of severe complication based on 9783 biopsies in Japan. Eur J Radiol 2006;59: Laspas F, Roussakis A, Efthimiadou R, Papaioannou D, Papadopoulos S, Andreou J. Percutaneous CT-guided fineneedle aspiration of pulmonary lesions: Results and complications in 409 patients. J Med Imaging Radiat Oncol 2008;52: Matsuguma H, Nakahara R, Kondo T, Kamiyama Y, Mori K, Yokoi K. Risk of pleural recurrence after needle biopsy in patients with resected early stage lung cancer. Ann Thorac Surg 2005;80: Heck SL, Blom P, Berstad A. Accuracy and complications in computed tomography fluoroscopy-guided needle biopsies of lung masses. Eur Radiol 2006;16: Ohno Y, Hatabu H, Takenaka D, Imai M, Ohbayashi C, Sugimura K. Transthoracic CT-guided biopsy with multiplanar reconstruction image improves diagnostic accuracy of solitary pulmonary nodules. Eur J Radiol 2004;51: Wisnivesky JP, Henschke CI, Yankelevitz DF. Diagnostic percutaneous transthoracic needle biopsy does not affect survival in stage I lung cancer. Am J Respir Crit Care Med 2006;174: Inoue M, Takakuwa T, Minami M, et al. Clinicopathologic factors influencing postoperative prognosis in patients with small-sized adenocarcinoma of the lung. J Thorac Cardiovasc Surg 2008;135: Inoue M, Minami M, Shiono H, Sawabata N, Ideguchi K, Okumura M. Clinicopathologic study of resected, peripheral, small-sized, non-small cell lung cancer tumors of 2 cm or less in diameter: pleural invasion and increase of serum carcinoembryonic antigen level as predictors of nodal involvement. J Thorac Cardiovasc Surg 2006;131: Sano Y, Date H, Toyoda S, et al. Percutaneous computed tomography-guided lung biopsy and pleural dissemination. Cancer 2009;115: Sawabata N, Ohta M, Maeda H. Fine-needle aspiration cytologic technique for lung cancer has a high potential of malignant cell spread through the tract. Chest 2000; 118: GENERAL THORACIC