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Thoracoscopic Fine-Needle Aspiration of Solitary Pulmonary Nodules
Thoracoscopic Fine-Needle Aspiration of Solitary Pulmonary Nodules Michael Bousamra II, MD, and Lawrence Clowry, Jr, MD Departments of Cardiothoracic Surgery and Pathology, Medical College of Wisconsin, Milwaukee, Wisconsin
To determine the diagnostic efficacy of thoracoscopic fine-needle aspiration (FNA) of solitary pulmonary nodules suspicious for lung cancer, we performed intraoperative thoracoscopic FNA for diagnostic purposes in 8 consecutive patients with peripheral solitary pulmonary nodules suspicious for lung cancer. Thoracoscopic FNA yielded an accurate diagnosis in all cases. There were 5 cases of non–small cell lung carcinoma, 1 small cell lung carcinoma, 1 renal carcinoma metastasis, and 1 inflammatory nodule. Results of FNA were obtained in less than 10 minutes in 6 cases. Maximum time to diagnosis was 20 minutes. The surgical procedure was expedited in the 6 cases of lung cancer because lobectomy followed
FNA rather than the performance of a diagnostic wedge resection. A minor hematoma after FNA was the single complication. Thoracoscopic FNA yielded a prompt and accurate diagnosis of peripheral solitary pulmonary nodules. Thoracoscopic FNA should be considered as an alternative to preoperative percutaneous FNA, which risks pneumothorax and patient discomfort. In cases of lung cancer, thoracoscopic FNA allows the surgeon to bypass a diagnostic wedge resection and to proceed with definitive lobectomy.
M
rapid and accurate diagnosis. Immediately after FNA diagnosis, formal resection can be performed. We prospectively studied the facility and accuracy of intraoperative FNA performed with thoracoscopic guidance with the expectation that it could expedite the surgical management of peripheral solitary pulmonary nodules suspected of being malignant.
anagement of the solitary pulmonary nodule is one of the most common problems encountered by physicians treating diseases of the chest. Lung cancer is clearly the prominent concern in these patients. Larger, central lesions lend themselves to bronchoscopic sampling whereas smaller, peripheral lesions are commonly approached by percutaneous fine-needle aspiration (FNA) under radiographic guidance. Because specific noncancerous diagnoses are rarely made by FNA, many clinicians advocate surgical wedge resection as the initial diagnostic and therapeutic modality for peripheral lesions. When lung cancer is diagnosed, wedge resection is followed by lobectomy and either lymph node dissection or lymph node sampling as standard therapy. The probability that a solitary pulmonary nodule is cancerous affects the aggressiveness of diagnostic endeavors. Low-suspicion lesions are frequently followed up by serial radiographs. Solitary pulmonary nodules that are spiculated, noncalcified, new or growing in size, and arising in patients with a smoking history are highly suspected of being lung cancer and should undergo definitive treatment as soon as possible. Thoracoscopic FNA of peripheral solitary pulmonary nodules has the potential to rapidly achieve a diagnosis without the attendant risk of pneumothorax and patient discomfort associated with preoperative percutaneous FNA. Intraoperative preparation of the sample by a trained cytotechnologist and subsequent microscopic evaluation by a skilled cytopathologist are essential for Accepted for publication April 24, 1997. Address reprint requests to Dr Bousamra, Department of Cardiothoracic Surgery, Froedtert Memorial Lutheran Hospital, PO Box 26099, Milwaukee, WI 53226-0099.
© 1997 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
(Ann Thorac Surg 1997;64:1191–3) © 1997 by The Society of Thoracic Surgeons
Technique Over an 18-month period, 8 patients underwent thoracoscopy with FNA of peripheral solitary pulmonary nodules suspected of being malignant. Patients presenting with a solitary pulmonary nodule that likely could be visualized via thoracoscopy were selected for thoracoscopic FNA. Initially a video thoracoscopic system was used. The thoracoscope was inserted in the sixth or seventh intercostal space in the midaxillary line and the lesion was visually identified. Appropriate portals were placed to grasp the lung and to insert a needle for FNA. This method was used in 2 patients and was found to be needlessly cumbersome. In all subsequent patients, a mediastinoscope was inserted into the intercostal space along the line of potential thoracotomy (Fig 1). The superficial pulmonary nodule was visualized directly in each instance. The mediastinoscope was brought in contact with the lung, and gentle sustained inflation fixed the area of pathology to the lumen of the scope. Controlled passage of a 22-gauge needle through the lumen of the mediastinoscope was then performed under direct vision. Fine-needle aspirates were fixed and stained in the operating room by a cytotechnologist using the “rapid pap” technique. They were then immediately sent to the 0003-4975/97/$17.00 PII S0003-4975(97)00813-8
1192
HOW TO DO IT BOUSAMRA AND CLOWRY THORACOSCOPIC FINE-NEEDLE ASPIRATION
Ann Thorac Surg 1997;64:1191–3
Table 1. Thoracoscopic Fine-Needle Aspiration Patient No.
Fig 1. Transthoracic insertion of the mediastinoscope allows direct visualization of the pulmonary nodule for fine-needle aspiration.
pathology department, where a cytopathologist reviewed the slide. We used the cyto stain technique: the FNA sample was immediately placed onto a glass slide, which was smeared against another slide to create two mirror image smears. These were then immediately placed in Carnoy’s fixative (30 seconds) to lyse red blood cells and begin cellular fixation. The slides were transferred to 95% ethanol (30 seconds) for final fixation. One of the slides was transferred to the rapid pap stain, and the other was retained in 95% ethanol for routine staining in the cytology laboratory after the surgical procedure. The rapid pap stain consisted of eight steps: distilled water, hematoxylin, distilled water and lithium carbonate, 95% ethanol, eosin cytoplasmic stain-50, 95% ethanol, 100% ethanol, and xylene. Each step took approximately 30 seconds, after which the slide was coverslipped and examined by the cytotechnologist for malignancy. A photomicrograph of a representative rapid pap slide is shown in Figure 2. A slide read as positive by the cytotechnologist was immediately transferred to the cytopathologist for final approval. If the FNA was negative
Location
Diagnosis
1
RLL
2
LUL
3 4 5 6 7 8
LUL RUL LUL LUL LUL RUL
Poorly differentiated CA suspect renal cell Poorly differentiated NSCLCA NSCLCA Adenocarcinoma (lung) Small cell CA NSCLCA NSCLCA Inflammatory
CA 5 cancer; lung cancer;
LUL 5 left upper lobe; RLL 5 right lower lobe;
Time (min) 20 ,10 ,10 ,10 ,10 ,10 ,10 20
NSCLCA 5 non–small cell RUL 5 right upper lobe.
for malignancy the surgeon was made aware that further sampling would be necessary given that malignancy was strongly suspected.
Results Thoracoscopic FNA was performed in 8 patients with peripheral solitary pulmonary nodules (Table 1). There were 5 cases of non–small cell carcinoma, 1 small cell carcinoma, 1 renal carcinoma metastasis, and 1 inflammatory nodule. The fine needle aspirate interpreted by the cytopathologist yielded an accurate diagnosis in all cases. Results of FNA were obtained in less than 10 minutes in 6 of the 8 thoracoscopic cases. There was one minor hemorrhage related to FNA when an 18-gauge needle was used for transthoracic aspiration. A hematoma developed within the lung after aspiration, and a small amount of blood was present in the endotracheal tube. Bleeding was easily controlled by placing a clamp across the pulmonary parenchyma proximal to the pulmonary nodule. Wedge resection of the nodule eliminated the problem. Subsequently, a 22-gauge needle was used for all aspirations.
Comment
Fig 2. Photomicrograph of a “rapid pap” stain demonstrating adenocarcinoma. Mucinous cytoplasm, large nuclei, and abundant nucleoli are seen.
Thoracoscopic FNA has its greatest utility in the diagnosis of peripheral pulmonary nodules that are suspected of being lung cancer and would require lobectomy after intraoperative diagnosis. Fine-needle aspiration during open thoracotomy has previously been shown to be safe and has accurately distinguished benign and malignant pathologies [1–3]. In this series, thoracoscopic FNA was an accurate diagnostic modality in the discernment of pulmonary malignancies. Selection of patients with peripheral lesions allowed easy localization at thoracoscopy and the ability to sample the lesion without traversing significant portions of normal lung. When lung cancer was suspected at the outset, FNA provided a prompt diagnosis, permitting the surgeon to directly proceed with lobectomy—the standard treatment for most patients with peripheral lung carcinoma. Thus, in the 6
Ann Thorac Surg 1997;64:1191–3
cases of lung carcinoma, FNA clearly expedited the intraoperative decision to perform lobectomy, which was carried out via thoracotomy. Notably, FNA was a redundant diagnostic procedure when wedge resection alone was the appropriate therapy, as with the inflammatory pulmonary nodule (patient 8) and metastatic renal lesion (patient 1). On the other hand, both frozen section and FNA have diagnostic limitations in the differentiation of lung cancer from metastatic cancer to the lung, and the combination of these two modalities increased the security of the intraoperative diagnosis in our patient with metastatic poorly differentiated renal cell carcinoma. Selective use of FNA during thoracoscopy can reduce costs. In our experience, thoracoscopic wedge resection of a 2- to 3-cm nodule requires the use of a single endoscopic stapling instrument and three or four staple cartridges. The cost ranges from $500 to $1,000 for materials alone. When one considers the 20 to 30 minutes required for video-assisted thoracoscopic resection, the instrumentation that accompanies it, and the greater time needed for frozen section preparation after wedge resection, the savings of thoracoscopic FNA become obvious. Intraoperative, thoracoscopic FNA also has advantages over preoperative, percutaneous FNA. The latter procedure subjects the patient to discomfort and anxiety and poses a variable risk of pneumothorax. Furthermore, during thoracoscopy, the surgeon has direct control of the lesion and can easily perform multiple aspirations of the nodule. Diagnostic accuracy for cancer is likely to reach 100% because the risk of pneumothorax is not present to counterweigh the need to achieve adequate sampling. Patient 2 was particularly notable in this regard because the left upper lobe tumor was surrounded by emphysematous bullae, which contraindicated percutaneous FNA (Fig 3). Selection of fine-gauged needles for FNA within the chest is appropriate. The use of fine-gauged needles has been associated with a negligible risk of tumor implantation during percutaneous procedures [4 – 6]. The same cannot be said of thoracoscopic wedge resection. Downey and associates [7] reported for the Video-Assisted Thoracic Surgery Study Group on 12 cases of pulmonary nodules resected thoracoscopically that later developed local recurrences in a pattern consistent with surgical tumor implantation. Twenty-one– gauge to 23-gauge needles are also less likely to result in hemorrhage if a vessel is traversed. The cytologic diagnostic yield with finegauged needles is equivalent to larger bore samples as has been demonstrated from FNA results from a variety of body sites [4]. In summary, thoracoscopic FNA is best employed in
HOW TO DO IT BOUSAMRA AND CLOWRY THORACOSCOPIC FINE-NEEDLE ASPIRATION
1193
Fig 3. Upper thoracic computed axial tomograph demonstrates a spiculated left upper lobe nodule adjacent to emphysematous bullae. Preoperative percutaneous fine-needle aspiration was not performed because of the risk of pneumothorax. Intraoperative thoracoscopic fine-needle aspiration yielded poorly differentiated non–small cell lung cancer.
peripheral lesions suspected of being lung cancer as FNA may obviate a diagnostic wedge resection. In this clinical setting thoracoscopic FNA was found to be an accurate, safe, and cost-effective diagnostic modality.
References 1. Capellari JO, Thompson EN III, Wallenhaupt SL. Utility of intraoperative fine needle aspiration biopsy in the surgical management of patients with pulmonary masses. Acta Cytol 1994;38:707–10. 2. Terada Y, Matsunobe S, Nemoto T, Tsuda T, Shimizu Y. Feasibility of intraoperative cytodiagnosis of lung cancer. Chest 1990;98:1156– 8. 3. DeCaro LF, Pak HY, Yokota S, Teplitz RL, Benfield JR. Intraoperative cytodiagnosis of lung tumors by needle aspiration. J Thorac Cardiovasc Surg 1983;85:404– 8. 4. Fry WA. Decision making at the time of exploratory thoracotomy. Ann Thorac Surg 1984;38:310–1. 5. Sagel SS, Ferguson TB, Forrest JV, Roper CL, Weldon CS, Clark RE. Percutaneous transthoracic aspiration needle biopsy. Ann Thorac Surg 1978;26:399 – 405. 6. Ljung BM. Techniques of aspiration and smear preparation. In: Koss LG, Woyke S, Olszewski W, eds. Aspiration biopsy: cytologic interpretation and histologic bases. 2nd Ed. New York: Igaku-Shoin, 1992:13. 7. Downey RJ, McCormack P, LoCicero J III, Video-Assisted Thoracic Surgery Study Group. Dissemination of malignant tumors after video-assisted thoracic surgery: a report of twenty-one cases. J Thorac Cardiovasc Surg 1996;111:954– 60.
To determine the diagnostic efficacy of thoracoscopic fine-needle aspiration (FNA) of solitary pulmonary nodules suspicious for lung cancer, we performed intraoperative thoracoscopic FNA for diagnostic purposes in 8 consecutive patients with peripheral solitary pulmonary nodules suspicious for lung cancer. Thoracoscopic FNA yielded an accurate diagnosis in all cases. There were 5 cases of non–small cell lung carcinoma, 1 small cell lung carcinoma, 1 renal carcinoma metastasis, and 1 inflammatory nodule. Results of FNA were obtained in less than 10 minutes in 6 cases. Maximum time to diagnosis was 20 minutes. The surgical procedure was expedited in the 6 cases of lung cancer because lobectomy followed
FNA rather than the performance of a diagnostic wedge resection. A minor hematoma after FNA was the single complication. Thoracoscopic FNA yielded a prompt and accurate diagnosis of peripheral solitary pulmonary nodules. Thoracoscopic FNA should be considered as an alternative to preoperative percutaneous FNA, which risks pneumothorax and patient discomfort. In cases of lung cancer, thoracoscopic FNA allows the surgeon to bypass a diagnostic wedge resection and to proceed with definitive lobectomy.
M
rapid and accurate diagnosis. Immediately after FNA diagnosis, formal resection can be performed. We prospectively studied the facility and accuracy of intraoperative FNA performed with thoracoscopic guidance with the expectation that it could expedite the surgical management of peripheral solitary pulmonary nodules suspected of being malignant.
anagement of the solitary pulmonary nodule is one of the most common problems encountered by physicians treating diseases of the chest. Lung cancer is clearly the prominent concern in these patients. Larger, central lesions lend themselves to bronchoscopic sampling whereas smaller, peripheral lesions are commonly approached by percutaneous fine-needle aspiration (FNA) under radiographic guidance. Because specific noncancerous diagnoses are rarely made by FNA, many clinicians advocate surgical wedge resection as the initial diagnostic and therapeutic modality for peripheral lesions. When lung cancer is diagnosed, wedge resection is followed by lobectomy and either lymph node dissection or lymph node sampling as standard therapy. The probability that a solitary pulmonary nodule is cancerous affects the aggressiveness of diagnostic endeavors. Low-suspicion lesions are frequently followed up by serial radiographs. Solitary pulmonary nodules that are spiculated, noncalcified, new or growing in size, and arising in patients with a smoking history are highly suspected of being lung cancer and should undergo definitive treatment as soon as possible. Thoracoscopic FNA of peripheral solitary pulmonary nodules has the potential to rapidly achieve a diagnosis without the attendant risk of pneumothorax and patient discomfort associated with preoperative percutaneous FNA. Intraoperative preparation of the sample by a trained cytotechnologist and subsequent microscopic evaluation by a skilled cytopathologist are essential for Accepted for publication April 24, 1997. Address reprint requests to Dr Bousamra, Department of Cardiothoracic Surgery, Froedtert Memorial Lutheran Hospital, PO Box 26099, Milwaukee, WI 53226-0099.
© 1997 by The Society of Thoracic Surgeons Published by Elsevier Science Inc
(Ann Thorac Surg 1997;64:1191–3) © 1997 by The Society of Thoracic Surgeons
Technique Over an 18-month period, 8 patients underwent thoracoscopy with FNA of peripheral solitary pulmonary nodules suspected of being malignant. Patients presenting with a solitary pulmonary nodule that likely could be visualized via thoracoscopy were selected for thoracoscopic FNA. Initially a video thoracoscopic system was used. The thoracoscope was inserted in the sixth or seventh intercostal space in the midaxillary line and the lesion was visually identified. Appropriate portals were placed to grasp the lung and to insert a needle for FNA. This method was used in 2 patients and was found to be needlessly cumbersome. In all subsequent patients, a mediastinoscope was inserted into the intercostal space along the line of potential thoracotomy (Fig 1). The superficial pulmonary nodule was visualized directly in each instance. The mediastinoscope was brought in contact with the lung, and gentle sustained inflation fixed the area of pathology to the lumen of the scope. Controlled passage of a 22-gauge needle through the lumen of the mediastinoscope was then performed under direct vision. Fine-needle aspirates were fixed and stained in the operating room by a cytotechnologist using the “rapid pap” technique. They were then immediately sent to the 0003-4975/97/$17.00 PII S0003-4975(97)00813-8
1192
HOW TO DO IT BOUSAMRA AND CLOWRY THORACOSCOPIC FINE-NEEDLE ASPIRATION
Ann Thorac Surg 1997;64:1191–3
Table 1. Thoracoscopic Fine-Needle Aspiration Patient No.
Fig 1. Transthoracic insertion of the mediastinoscope allows direct visualization of the pulmonary nodule for fine-needle aspiration.
pathology department, where a cytopathologist reviewed the slide. We used the cyto stain technique: the FNA sample was immediately placed onto a glass slide, which was smeared against another slide to create two mirror image smears. These were then immediately placed in Carnoy’s fixative (30 seconds) to lyse red blood cells and begin cellular fixation. The slides were transferred to 95% ethanol (30 seconds) for final fixation. One of the slides was transferred to the rapid pap stain, and the other was retained in 95% ethanol for routine staining in the cytology laboratory after the surgical procedure. The rapid pap stain consisted of eight steps: distilled water, hematoxylin, distilled water and lithium carbonate, 95% ethanol, eosin cytoplasmic stain-50, 95% ethanol, 100% ethanol, and xylene. Each step took approximately 30 seconds, after which the slide was coverslipped and examined by the cytotechnologist for malignancy. A photomicrograph of a representative rapid pap slide is shown in Figure 2. A slide read as positive by the cytotechnologist was immediately transferred to the cytopathologist for final approval. If the FNA was negative
Location
Diagnosis
1
RLL
2
LUL
3 4 5 6 7 8
LUL RUL LUL LUL LUL RUL
Poorly differentiated CA suspect renal cell Poorly differentiated NSCLCA NSCLCA Adenocarcinoma (lung) Small cell CA NSCLCA NSCLCA Inflammatory
CA 5 cancer; lung cancer;
LUL 5 left upper lobe; RLL 5 right lower lobe;
Time (min) 20 ,10 ,10 ,10 ,10 ,10 ,10 20
NSCLCA 5 non–small cell RUL 5 right upper lobe.
for malignancy the surgeon was made aware that further sampling would be necessary given that malignancy was strongly suspected.
Results Thoracoscopic FNA was performed in 8 patients with peripheral solitary pulmonary nodules (Table 1). There were 5 cases of non–small cell carcinoma, 1 small cell carcinoma, 1 renal carcinoma metastasis, and 1 inflammatory nodule. The fine needle aspirate interpreted by the cytopathologist yielded an accurate diagnosis in all cases. Results of FNA were obtained in less than 10 minutes in 6 of the 8 thoracoscopic cases. There was one minor hemorrhage related to FNA when an 18-gauge needle was used for transthoracic aspiration. A hematoma developed within the lung after aspiration, and a small amount of blood was present in the endotracheal tube. Bleeding was easily controlled by placing a clamp across the pulmonary parenchyma proximal to the pulmonary nodule. Wedge resection of the nodule eliminated the problem. Subsequently, a 22-gauge needle was used for all aspirations.
Comment
Fig 2. Photomicrograph of a “rapid pap” stain demonstrating adenocarcinoma. Mucinous cytoplasm, large nuclei, and abundant nucleoli are seen.
Thoracoscopic FNA has its greatest utility in the diagnosis of peripheral pulmonary nodules that are suspected of being lung cancer and would require lobectomy after intraoperative diagnosis. Fine-needle aspiration during open thoracotomy has previously been shown to be safe and has accurately distinguished benign and malignant pathologies [1–3]. In this series, thoracoscopic FNA was an accurate diagnostic modality in the discernment of pulmonary malignancies. Selection of patients with peripheral lesions allowed easy localization at thoracoscopy and the ability to sample the lesion without traversing significant portions of normal lung. When lung cancer was suspected at the outset, FNA provided a prompt diagnosis, permitting the surgeon to directly proceed with lobectomy—the standard treatment for most patients with peripheral lung carcinoma. Thus, in the 6
Ann Thorac Surg 1997;64:1191–3
cases of lung carcinoma, FNA clearly expedited the intraoperative decision to perform lobectomy, which was carried out via thoracotomy. Notably, FNA was a redundant diagnostic procedure when wedge resection alone was the appropriate therapy, as with the inflammatory pulmonary nodule (patient 8) and metastatic renal lesion (patient 1). On the other hand, both frozen section and FNA have diagnostic limitations in the differentiation of lung cancer from metastatic cancer to the lung, and the combination of these two modalities increased the security of the intraoperative diagnosis in our patient with metastatic poorly differentiated renal cell carcinoma. Selective use of FNA during thoracoscopy can reduce costs. In our experience, thoracoscopic wedge resection of a 2- to 3-cm nodule requires the use of a single endoscopic stapling instrument and three or four staple cartridges. The cost ranges from $500 to $1,000 for materials alone. When one considers the 20 to 30 minutes required for video-assisted thoracoscopic resection, the instrumentation that accompanies it, and the greater time needed for frozen section preparation after wedge resection, the savings of thoracoscopic FNA become obvious. Intraoperative, thoracoscopic FNA also has advantages over preoperative, percutaneous FNA. The latter procedure subjects the patient to discomfort and anxiety and poses a variable risk of pneumothorax. Furthermore, during thoracoscopy, the surgeon has direct control of the lesion and can easily perform multiple aspirations of the nodule. Diagnostic accuracy for cancer is likely to reach 100% because the risk of pneumothorax is not present to counterweigh the need to achieve adequate sampling. Patient 2 was particularly notable in this regard because the left upper lobe tumor was surrounded by emphysematous bullae, which contraindicated percutaneous FNA (Fig 3). Selection of fine-gauged needles for FNA within the chest is appropriate. The use of fine-gauged needles has been associated with a negligible risk of tumor implantation during percutaneous procedures [4 – 6]. The same cannot be said of thoracoscopic wedge resection. Downey and associates [7] reported for the Video-Assisted Thoracic Surgery Study Group on 12 cases of pulmonary nodules resected thoracoscopically that later developed local recurrences in a pattern consistent with surgical tumor implantation. Twenty-one– gauge to 23-gauge needles are also less likely to result in hemorrhage if a vessel is traversed. The cytologic diagnostic yield with finegauged needles is equivalent to larger bore samples as has been demonstrated from FNA results from a variety of body sites [4]. In summary, thoracoscopic FNA is best employed in
HOW TO DO IT BOUSAMRA AND CLOWRY THORACOSCOPIC FINE-NEEDLE ASPIRATION
1193
Fig 3. Upper thoracic computed axial tomograph demonstrates a spiculated left upper lobe nodule adjacent to emphysematous bullae. Preoperative percutaneous fine-needle aspiration was not performed because of the risk of pneumothorax. Intraoperative thoracoscopic fine-needle aspiration yielded poorly differentiated non–small cell lung cancer.
peripheral lesions suspected of being lung cancer as FNA may obviate a diagnostic wedge resection. In this clinical setting thoracoscopic FNA was found to be an accurate, safe, and cost-effective diagnostic modality.
References 1. Capellari JO, Thompson EN III, Wallenhaupt SL. Utility of intraoperative fine needle aspiration biopsy in the surgical management of patients with pulmonary masses. Acta Cytol 1994;38:707–10. 2. Terada Y, Matsunobe S, Nemoto T, Tsuda T, Shimizu Y. Feasibility of intraoperative cytodiagnosis of lung cancer. Chest 1990;98:1156– 8. 3. DeCaro LF, Pak HY, Yokota S, Teplitz RL, Benfield JR. Intraoperative cytodiagnosis of lung tumors by needle aspiration. J Thorac Cardiovasc Surg 1983;85:404– 8. 4. Fry WA. Decision making at the time of exploratory thoracotomy. Ann Thorac Surg 1984;38:310–1. 5. Sagel SS, Ferguson TB, Forrest JV, Roper CL, Weldon CS, Clark RE. Percutaneous transthoracic aspiration needle biopsy. Ann Thorac Surg 1978;26:399 – 405. 6. Ljung BM. Techniques of aspiration and smear preparation. In: Koss LG, Woyke S, Olszewski W, eds. Aspiration biopsy: cytologic interpretation and histologic bases. 2nd Ed. New York: Igaku-Shoin, 1992:13. 7. Downey RJ, McCormack P, LoCicero J III, Video-Assisted Thoracic Surgery Study Group. Dissemination of malignant tumors after video-assisted thoracic surgery: a report of twenty-one cases. J Thorac Cardiovasc Surg 1996;111:954– 60.