Need for Preoperative Computed Tomography-Guided Localization in Video-Assisted Thoracoscopic Surgery Pulmonary Resections of Metastatic Pulmonary Nodules

Need for Preoperative Computed Tomography-Guided Localization in Video-Assisted Thoracoscopic Surgery Pulmonary Resections of Metastatic Pulmonary Nodules GENERAL THORACIC

Shinji Nakashima, MD, PhD, Atsushi Watanabe, MD, PhD, Takuro Obama, MD, Gen Yamada, MD, PhD, Hiroki Takahashi, MD, PhD, and Tetsuya Higami, MD, PhD Department of Thoracic and Cardiovascular Surgery, and Third Department of Internal Medicine, Sapporo Medical University School of Medicine, Sapporo, Japan

Background. Preoperative localization of pulmonary nodules is sometimes necessary when they are too small or distant from the surface of the visceral pleura to be detected during video-assisted thoracoscopic surgery. This study aims to present the criteria for localization and to evaluate the accuracy of the criteria. Methods. From April 2001 to March 2008, 178 patients with 224 nodules who underwent wedge resection of pulmonary metastatic nodules by video-assisted thoracoscopic surgery were reviewed retrospectively. Thirty-one patients (17.4%) including 35 nodules underwent thoracoscopic resection immediately after computed tomography– guided localization using hook wires. Criteria for preoperative localization were (1) maximum diameter of the nodule of 5 mm or less, (2) maximum diameter to minimum distance between the visceral pleura and inferior border of nodule of 0.5 or less, and (3) nodule with low-density image by computed tomography after che-

motherapy. The accuracy of these inclusion criteria was statistically evaluated. Results. All 224 nodules were removed by wedge resection or additional segmentectomy. Nineteen nodules (54.3%) were detected in the thoracic cavity with preoperative localization. Sensitivity, specificity, positive predictive value, and negative predictive value were 11.1%, 99.5%, 66.7%, and 92.8%; 88.9%, 93.2%, 53.3%, and 99.0%; and 88.9%, 90.8%, 45.7%, and 98.9% in each preoperative finding of which a nodule met all (3 nodules), two or more (30 nodules), and one or more (35 nodules) of the three criteria, respectively. Conclusions. This study suggests that preoperative localization should be considered before video-assisted thoracoscopic surgery operation if the pulmonary nodule meets two or more of our criteria. (Ann Thorac Surg 2010;89:212–9) © 2010 by The Society of Thoracic Surgeons

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ecause of the widespread clinical use of helical computed tomography (CT), there is an increase in the radiologic detection rate of small pulmonary nodules. These nodules were previously undetectable by means of conventional CT. The advances in diagnostic technology have further emphasized the role of video-assisted thoracoscopic surgery (VATS) for small pulmonary nodules. Although a VATS operation is safe and minimally invasive, some pulmonary nodules are difficult to identify thoracoscopically. The difficulty in locating small or deeply situated target nodules has been the major limiting factor in the success of thoracoscopic resection. Therefore, preoperative localization of the nodules is necessary when they are too small or too distant from the surface of the visceral pleura to be detected during VATS resection [1, 2].

Although published articles on the methods and indications for preoperative localization are available, the reports include primary lung cancer, metastatic lung cancer, and benign pulmonary nodules [1– 4]. However, the surgical strategies for primary lung cancer are completely different from those for metastatic lung cancer [5, 6]. The criteria for preoperative localization should also be different between primary lung cancer and metastatic lung cancer [6]. Therefore, we focused on wedge resection of a single or multiple metastatic pulmonary nodules by VATS and assessed the criteria for preoperative localization. We performed a retrospective review of patients with metastatic pulmonary nodules and assessed the inclusion criteria for preoperative hook wire placement on the basis of the preoperative CT findings.

Accepted for publication Sept 29, 2009.

Patients and Methods

Address correspondence to Dr Nakashima, Department of Thoracic and Cardiovascular Surgery, Sapporo Medical University School of Medicine, South 1, West 16, Chuo-ku, Sapporo, 060-8543, Japan; e-mail: nakashim@ sapmed.ac.jp.

The institutional review board approved the retrospective data retrieval, which entailed that informed consents were waived. From the period of April 2001 through

© 2010 by The Society of Thoracic Surgeons Published by Elsevier Inc

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Table 1. Patient and Nodule Characteristics

be identified by their location during thoracoscopy. Additionally, in reference to some reports [1, 2], three clinical criteria for preoperative localization were developed on the basis of the following preoperative CT findings: (1) maximum diameter of nodule of 5 mm or less, (2) maximum diameter to minimum distance between the visceral pleura and inferior border of the nodule of 0.5 or less (Fig 1), and (3) low-density image of the nodule after chemotherapy (Fig 2). Thirty-one patients (17.4%) with a total of 35 nodules underwent thoracoscopic resection of a single or multiple pulmonary nodules immediately after CT-guided localization using hook wire needles (Guiding Marker System; Hakko Medical Products, Tokyo, Japan). The comparison between the two groups as to nodules with and without preoperative localization is shown in Table 2. No significant relationship was observed between the two groups regarding lobar or segmental location of the lesions.

Characteristic Number of patients (nodules) Age (y) Sex (male/female) Pathologic diagnosis Colon cancer Testicular cancer Renal cell cancer Breast cancer Osteosarcoma Other Nodule location Right Lower lobe Right upper Middle Lower Left upper apical Lingular Lower

Undetectable Group

Detectable Group

16 (18)

162 (206)

49 ⫾ 8 11/5

51 ⫾ 12 92/70

3 3 3 2 1 4

46 10 13 10 20 63

7 10 2 2 5 4 0 5

124 89 46 28 50 36 7 39

p Value

0.411 0.355

0.333 0.087

March 2009, the study population consisted of 178 patients (103 men and 75 women), whose age ranged from 19 to 82 years (mean, 53 years) with a total of 224 nodules. All patients underwent thoracoscopic wedge resection of a single or multiple pulmonary metastatic nodules in our institute. The patients were assigned to two groups: (1) undetectable group and (2) detectable group. The undetectable group was composed of 16 patients with imperceptible nodules (including the nodules detected by CT-guided nodule localization). On the other hand, the detectable group was composed of 162 patients, who had overt nodules even without preoperative CT-guided localization. The comparison between the two groups as to age, sex, histopathologic diagnosis, and locations of the nodules is shown in Table 1. No significant relationship was observed between the two groups regarding histologic results and lobar or segmental location of the lesions.

Criteria for Preoperative Computed Tomographic–Guided Localization of the Nodules The chest CT scan images were carefully examined preoperatively to determine whether the nodules could

Operative Procedure Thoracoscopic surgery was performed under general anesthesia using single-lung ventilation by means of a dual-lumen endobronchial tube. The thoracoscope was inserted through a thoracic port with the incision in the seventh intercostal space midaxillary line in most patients. Additional intercostal incisions were made for resection and manipulation of the lesion as necessary. Identification of the nodules was attempted by 2 thoracic surgeons among the authors. Preoperative placement of the hook wire allowed easy determination of the nodules’ location during thoracoscopic surgery. Once the nodules were identified, thoracoscopic wedge resections were performed. If the nodules were neither visible thoracoscopically nor palpable with the surgeon’s finger through a port or through a minithoracotomy even after preoperative localization, thoracoscopic extended wedge resections, including the hook wire, were performed; and the nodules in the specimens were confirmed. When the nodules could not be identified in the thoracic cavity, the nodules were defined as undetectable nodules during operation. After resection of the small pulmonary nodules, histologic examination was immediately performed on all specimens. If malignant involvement of the surgical margin was observed or the nodules were undetectable during operation even after histologic examination of specimens, additional segmentectomy or wedge resection was performed. Fig 1. Criteria for preoperative localization. 1) Maximum diameter of nodule (A) of 5 mm or less. 2) Maximum diameter of nodules (A) to minimum distance between the visceral pleura and inferior border of nodule (B) of 0.5 or less.

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Fig 2. Chest computed tomograms showing metastatic pulmonary nodules of bladder cancer origin. (A) Solid nodule with high-density image before chemotherapy. (B) Faint nodule with low-density image after chemotherapy, which needs preoperative localization.

GENERAL THORACIC

Data and Statistical Analysis The statistical analysis was performed using SPSS 11.0 software (SPSS Inc, Chicago, IL). Values were expressed as mean ⫾ standard deviations. The ␹2 test and twotailed unpaired Student’s t test were used when appropriate to compare the results between the two groups. Differences were considered significant when the probability value was less than 0.05. Receiver operating characteristic (ROC) curve analysis was performed to assess the prediction ability of identifying the diameter factor (criterion 1) and depth factor (criterion 2) of undetectable nodules. We used a cutoff value on the scale of the predicted probabilities from logistic regression to classify nodules into two groups on the basis of intraoperative detectability: undetectable group and detectable group. The objective was to select a cutoff point with sufficiently high sensitivity and specificity for distinction between undetectable and detectable nodules. The relationship between the sensitivity and the specificity of various cutoff points can be plotted as an ROC curve for each criterion factor. The sensitivity, specificity, positive predictive value, and negative predictive value in the estimation of our aggregate criteria for preoperative CT-guided nodule localization requirement were defined as follows: sensitivity is the ratio of the number of undetectable nodules that meet the aggregate criteria to all undetectable nodules; specificity is the ratio of the number of detectable nodules that do not meet the aggregate criteria to all detectable nodules; positive predictive value is the ratio of the number of undetectable nodules that meet the aggreTable 2. Nodule Locations With or Without Localization

Location Right Lower lobe Right upper Middle Lower Left upper apical Lingular Lower

With Localization (n ⫽ 35)

Without Localization (n ⫽ 189)

17 17 4 4 9 9 1 8

116 82 44 26 46 30 7 36

p Value 0.192 0.584

gate criteria to all nodules that meet the aggregate criteria; and negative predictive value is the ratio of the number of detectable nodules that do not meet the aggregate criteria to all nodules that do not meet the aggregate criteria.

Results Preoperative localization of the pulmonary nodules was performed on 31 of 178 patients (17.4%), which included 35 of 224 nodules (15.6%). Of the 35 nodules, 3 nodules met three of three criteria, 27 nodules met two of three criteria (criteria 1⫹2, 20 nodules; criteria 2⫹3, 7 nodules), and 5 nodules fulfilled only one criterion (criterion 1, 2 nodules; criterion 2, 3 nodules; Table 3). The maximum diameter of the nodules was 4.9 ⫾ 1.8 mm. The maximum diameter to minimum distance between the visceral pleura and inferior border of the nodule was 0.35 ⫾ 0.13. There were 7 of 18 nodules with low-density image after chemotherapy (Table 4). During preoperative localization, the minimum distance between the body surface and tip of the wire needle was 59.7 ⫾ 19.0 mm, the minimum distance between the pleural surface and tip of the wire needle was 18.1 ⫾ 11.0 mm, and the minimum distance between the nodule and tip of the hook wire was 8.6 ⫾ 7.0 mm.

Operative Findings The preoperative localization did not cause any serious complications in all 31 patients. Conversion to thoracotomy because of the inability to detect the nodules or any other reasons did not occur. No additional wedge resection or segmentectomy for preoperative localization was performed because of the absence of nodules in the specimens. During the operation for preoperatively localized nodules, 19 nodules (54.3%) were identified without the need for preoperative hook wire needles (Table 3). One nodule that met all three criteria, 13 that met two criteria of three, and 4 that met only one criterion were palpable in the thoracic cavity. In addition, one other nodule that met only one criterion was visible by thoracoscopy from the interlobar aspect. Even though some nodules localized preoperatively were not detected in the thoracic cavity, all nodules were detected in the specimens after wedge resection, including a hook wire.

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Table 3. Operative Findings of Nodules

Operative Finding Number of nodules Criteria met Detectable in thoracic cavity Visible by thoracoscopy Palpable in thoracic cavity Undetectable after wedge resection Necessity for preoperative localization

3

2

1

0

3 1⫹2⫹3; 3 nodules 1 0 1 0 2

27 1⫹2; 20 nodules, 2⫹3; 7 nodules 13 0 13 0 14

5 1; 2 nodules, 2; 3 nodules 5 1 4 0 0

189 0 nodules 187 51 136 2 2

Criterion: 1) maximum diameter of the nodule ⬍ 5 mm; 2) maximum diameter/minimum distance between the visceral pleura and the inferior border of nodule ⬍ 0.5; 3) nodule with low-density image by computed tomography after chemotherapy.

On the other hand, two nodules, which did not fulfill even one criterion, were not identified in the surgical specimens after wedge resection; thus, additional segmentectomy was required. One nodule was located at the posterior segment of the right upper lobe (segment 2), and another nodule was located at the apical segment of the left upper lobe (segment 1⫹2). All other nonlocalized nodules were detected in the thoracic cavity and further identified in the resected specimens.

Analysis and Assessment of Our Criteria for Preoperative Localization Requirement The ROC analysis for maximum diameter factor (criterion 1) and depth factor (criterion 2), which indicated the overall prediction ability of identifying an undetectable nodule, was sufficiently high because the areas under the curves were close to 1.0 (maximum diameter factor, 0.898 and depth factor, 0.944; Fig 3). The cutoff point for criterion 1 was 5 mm diameter. In this condition, the sensitivity and specificity from ROC analysis were 90.8% and 72.2%, respectively. The cutoff point for criterion 2 was 0.5. In this condition, the sensitivity and specificity from ROC analysis were 79.1% and 88.9%, respectively. The sensitivity, specificity, positive predictive value, and negative predictive value in the estimation of the aggregate criteria for preoperative nodule localization requirement are shown in Table 5. According to the Table 4. Profiles of the Nodules

Profile Maximum diameter (mm) Maximum diameter/ minimum distance between the visceral pleura and inferior border of nodule Low-density image after chemotherapy

Undetectable Group (n ⫽ 18)

Detectable Group (n ⫽ 206)

p Value

4.9 ⫾ 1.8

10.2 ⫾ 7.1

⬍0.001

0.35 ⫾ 0.13

0.62 ⫾ 0.99

⬍0.001

7

3

⬍0.001

analysis of data, when all three criteria were met, the sensitivity was 11.1%, which was relatively low for identification of small nodules by VATS. The specificity was 99.5% and positive predictive value was 66.7% in this condition. On the other hand, when one criterion or more were fulfilled, the sensitivity was 88.9%, which was the same when two or more criteria were met. In addition, the specificity of the former was 90.8%, which was lower than the latter condition, and positive predictive value was relatively low at 45.7%.

Comment In recent years, the indications and capabilities of thoracoscopic surgery have been broadened as the results of improved video options and surgical instruments [6]. One of the limiting factors in thoracoscopic resection of the lung is the inability to determine the exact location of a target pulmonary nodule that is either small or located far below the pleural surface [1–3, 7–9]. Paci and colleagues [7] reported that peripheral nodules with diameters of less than 1 cm were candidates for preoperative localization. Eichfeld and associates [8] reported that subpleural nodules with a maximum distance from the pleura of more than 3 cm was another indication. If judged to be too small or too deep beneath the pleural surface to be seen or palpated during VATS resection, the nodules must be localized preoperatively [7, 9]. Otherwise, additional segmentectomy or conversion to open thoracotomy was warranted for small pulmonary nodules when detection of the exact location failed. Although there have been published articles on the methods and indications for preoperative localization in pulmonary resection by VATS [1– 4, 6 –9], the reports included primary lung cancer, metastatic lung cancer, and benign pulmonary nodules. Some primary lung cancers that cannot be palpated easily by VATS, such as the nodules of adenocarcinoma with ground-glass opacity, might require preoperative localization. When the nodules cannot be identified in the thoracic cavity, segmentectomy for diagnostic or therapeutic purposes from the beginning of the operation is sometimes required. This signifies that the indications and criteria for preop-

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Number of Criteria Met

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Fig 3. Receiver operating characteristics curves for maximum diameter factor, criterion 1 (A) and depth factor, criterion 2 (B).

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erative localization should be different between primary lung cancer and metastatic lung cancer. Because the definitive pathologic diagnoses are sometimes different from the preoperative diagnoses, we exclude many patients with indeterminate pulmonary nodules based on the pathologic findings of benign pulmonary tumor, primary lung cancer, or other diseases. In addition, we have to resect the metastatic pulmonary nodules after chemotherapy as therapeutic, diagnostic, and prognostic of the residual tumor. In this condition, pulmonary nodules after chemotherapy sometimes present with faint and low-density images, such as the case of ground-glass opacity. Hence, it is difficult for surgeons to detect these nodules without preoperative localization. In this study, we focused on metastatic pulmonary nodules and assessed our criteria for preoperative localization. There are numerous reports on the criteria for preoperative localization [1, 2, 7–9]. The nodules’ size and depth from the pleura are considered. Several of the indications are in concurrence with our study. Depth is not only the distance from the visceral pleura but also the ratio between nodule size and distance from the surface. Nodules large enough appear to be palpable even if

located deeply. Saito and coworkers [1] reported a linear function in terms of the nodules’ size and depth. Based on the results of these studies, criterion 1 for maximum diameter factor and criterion 2 for depth factor were applied in this study. The cutoff points for criterion 1 and criterion 2, which were decided by the ROC analysis, are acceptable for clinical decisions. In addition, the characteristics (hard or soft, solid or faint) of the nodules should be considered as an indication. If the nodules are solid, endoscopic identification might be possible because pulmonary nodules bulge against the surrounding atelectatic lung. Palpation with thoracoscopic instruments or the surgeon’s finger is the first means of detecting the nodules when the nodule cannot be identified visually. However, some types of nodules, such as localized bronchiole-alveolar carcinoma (nodules with ground-glass opacity), are difficult to locate, even if large or close to the pleural surface. The character is very soft, small, faint, and with similar consistency to the surrounding normal lung parenchyma. Therefore, we propose criterion 3 for metastatic pulmonary nodules, which is the low-density image of the nodules after chemotherapy by CT findings. This crite-

Table 5. Analysis and Assessment of Aggregate Criteria for Preoperative Localization Requirementa Preoperative Localization Requirement Aggregate Criteria All 3 criteria Yes No Total 2 criteria or more Yes No Total 1 criterion or more Yes No Total a

Yes

No

Total

2 16 18

1 205 206

3 221 224

16 2 18

14 192 206

30 194 224

16 2 18

19 187 206

35 189 224

See text for definitions of sensitivity, specificity, PPV, and NPV.

NPV ⫽ negative predictive value;

PPV ⫽ positive predictive value.

Sensitivity (%)

Specificity (%)

PPV (%)

NPV (%)

11.1

99.5

66.7

92.8

88.9

93.2

53.3

99.0

88.9

90.8

45.7

98.9

NAKASHIMA ET AL CT-GUIDED LOCALIZATION IN VATS METASTASECTOMY

rion is unique and might improve the detection of nodules. Even if pulmonary nodules are diagnosed as metastatic, CT findings of low density, such as the case of ground-glass opacity especially after chemotherapy, are evident. These nodules are difficult to detect because they are too soft and faint. Preoperative localization is necessary for this type of nodule. On the other hand, some types of nodules, like osteosarcoma in origin, are easy to detect in the thoracic cavity because the nodule is very solid and hard. In fact, two of five nodules, which met only one criterion and were detected in the thoracic cavity without preoperative localization, were metastatic osteosarcoma in the lung. These histologic factors should be considered in a future study. In the clinical setting, this kind of decision is often made on the basis of the experience of the thoracic surgeon in charge. Therefore, additional studies are necessary to determine what factors would be predictive for detectability of pulmonary nodules and the necessity for preoperative localization. Although it may be difficult to establish more appropriate criteria, our study would be helpful in such clinical settings. Our results suggest that nodules fulfilling two or more criteria are candidates for preoperative localization. As such, all analyzed data are acceptable and reasonable for preoperative localization. Based on the operative findings, nodules that meet only one criterion are not considered candidates for preoperative localization. This condition might indicate the need to defer preoperative localization. When nodules meet all three criteria, the sensitivity is 11.1%. This set of criteria is too strict and not suitable for clinical decision making. In addition, according to operative findings in Table 3, the clinical situation in which only one criterion was met did not require preoperative localization because all nodules in this study could be detected in the thoracic cavity without prior localization. If preoperative localization is less invasive, clinical conditions for the indication for localization should be broadened. However, this method imposes several potential slight and fatal complications [1– 4, 10, 11]. Therefore, operative findings and data analysis suggest that preoperative localization should be considered before VATS operation if the pulmonary nodule fulfills two or more of our criteria. Our results also suggest that all nodules can be detected intraoperatively when preoperative localization is performed. In our operative procedures, hook wire localization is an efficient method to facilitate intraoperative localization of small, deep-seated lesions. On the other hand, two nonlocalized nodules, which were relatively small and deep but did not meet even a single criterion, could not be identified after wedge resection. The diameters were 6 mm and 7 mm with locations in right segment 2 and left segments 1⫹2, respectively. The depth of both nodules was not significant. Although they were not peripherally located, it was difficult for the surgeon to palpate them through the minithoracotomy. These cases indicate that other conditions might influence difficulties in the detection of pulmonary nodules. For example, lesions in the segments that are difficult to detect and to

resect, such as basilar segments of the lower lobe, may require preoperative localization even if only one criterion or other conditions are met. On the other hand, if the lesions are in segments that are easy to detect technically (such as the right middle lobe or lingula of the left lung), preoperative localization might be not needed even if pleural criteria are met. Unexpectedly, our data showed that there was no significant difference among the locations of the nodules. However, additional criteria should be assessed for other conditions, for example, lobular or segmental location, preoperative pathologic diagnosis, and pleural or parenchymal conditions, such as emphysema or interstitial pneumonia, in future studies. In this study, CT-guided preoperative localization techniques using hook wires for pulmonary localization have been classified into three types. The first type uses an intraoperative imaging, either intraoperative ultrasonography [8, 12–14] or intraoperative navigation system [15]. The second class of targeting technique includes percutaneous injection of dyes [16], contrast media [17], radionuclides [18], and colored adhesive agents [19], or percutaneous hook wire [3, 10, 11] or wire coil placement [20 –23]. The third class of targeting technique includes transbronchial localization [24]. All methods have beneficial points and disadvantages [4, 9, 24, 25]. Percutaneous localization using hook wire needle is one of the most common methods used. However, preoperative localization using hook wire is also not completely safe and less invasive. Incidences of preoperative wire dislodgement with associated pneumothorax, intrapulmonary hemorrhage, and pleural pain have been reported with this technique. Mild pneumothorax often occurs if there is no pleural adhesion to the chest wall [3, 10]. Therefore, hook wire placement is performed within 1 hour before induction of general anesthesia with a double-lumen endotracheal tube. Single-lung ventilation immediately after intubation enables us to avoid tension pneumothorax and arterial air embolism by positive-pressure ventilation. Furthermore, hydration, head-down position, and reduction of positive airway pressure reduce the occurrence of arterial embolism.

Limitations First, this is a retrospective single-institution study. A retrospective analysis is susceptible to various sources of bias, which may not have been identified and controlled. Second, criteria 1 and 2 are quantitative and are completely objective; but criterion 3 is qualitative and is relatively unclear. It is difficult to precisely explain the definition of criterion 3. Finally, the size and location of minithoracotomy are very important in the identification of nodules intraoperatively by VATS. Minithoracotomy is usually 35 to 40 mm in length, and the location depends on where the nodule is situated. These issues should be considered.

Conclusions Preoperative localization using hook wires is useful in the reduction of operative difficulties for detection of nodules by VATS without any serious complications. This study

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suggests that preoperative localization should be considered before VATS operation if the pulmonary nodule meets two or more of our criteria.

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INVITED COMMENTARY The article by Nakashima and colleagues [1] is a very important contribution to our armamentarium regarding the diagnosis and treatment of small lung nodules. This is a burgeoning problem with the change in epidemiology of lung cancer and the ubiquity of chest computed tomography scans. Clearly, we are curing smaller, screening-detected-type lung cancers with a much higher rate than those that are picked up once symptoms occur. This gives all of us who treat patients with lung cancer much about which to be optimistic. However, we are faced with how best to handle the management of these small nodules. If they are malignant, we want to resect them as early as possible to give © 2010 by The Society of Thoracic Surgeons Published by Elsevier Inc

the highest chance of cure, as noted by Henschke and colleagues in the New England Journal of Medicine [2]. Although it is an uncommon situation, some of these small lesions can be difficult to identify in the operating room, making biopsy challenging. The method described by Nakashima and colleagues appears to be safe and effective. Going forward, it would be useful to conduct a prospective trial to better characterize the details of the lesions that are most benefited by this approach. Centrally located ground glass lesions in areas of the lung that are not amenable to a simple segmental resection (ie, basilar lower lobe) may be the ones most likely to need 0003-4975/10/$36.00 doi:10.1016/j.athoracsur.2009.11.002