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Right arrow Lung - cancer

Ann Thorac Surg 2004;77:1756-1762
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

A novel technique for localization and excisional biopsy of small or Ill-defined pulmonary lesions

Thomas M. Daniel, MDa*, Talissa A. Altes, MDb, Patrice K. Rehm, MDb, Mark B. Williams, PhDb, David R. Jones, MDa, Alexander V. Stolin, MSc, Spencer B. Gay, MDb

a Department of Surgery, Charlottesville, VA, USA
b Department of Radiology, Charlottesville, VA, USA
c Department of Physics, University of Virginia Health System, Charlottesville, Virginia, USA

Accepted for publication October 24, 2003.

* Address reprint requests to Dr Daniel, Department of Surgery, Box 800679, University of Virginia Health System, Charlottesville, VA 22908-0679, USA.
e-mail: tmd5m{at}virginia.edu


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The purpose of this study was to develop and evaluate radiotracer-guided localization of small or ill-defined pulmonary nodules for thoracoscopic excisional biopsy.

METHODS: This study consisted of two parts: a laboratory study in rats to determine the most suitable radiotracer, and a pilot study in humans to determine the feasibility of radiotracer lung nodule localization. The right lung of 12 rats was injected with a technetium 99m (Tc 99m) based radiotracer solution: 4 each with macroaggregated albumin (MAA), unfiltered sulfur colloid (SC), and pertechnetate (TcO4). Serial imaging was performed using a small animal gamma camera for 4 hours following injection. In 13 patients, computed tomographic (CT) guided injection of Tc 99m MAA solution was made into or adjacent to a pulmonary nodule suspicious for primary lung cancer. Gamma probe localization of the nodule was performed during subsequent thoracoscopic surgery.

RESULTS: In the animal model, MAA provided more precise localization than SC or TcO4 and was selected for the human study. In the human series, all 13 patients had successful gamma probe localization of their lesion. There were no radiologic or surgical complications. Seven of 13 nodules were malignant, and five of these nodules were stage IA primary lung carcinomas.

CONCLUSIONS: Computed tomographic-guided radiotracer localization of small or ill-defined pulmonary nodules using Tc 99 m MAA before thoracoscopic excisional biopsy is feasible and may make excisional biopsy the preferred management strategy for the management of small pulmonary nodules in patients at high risk for malignancy.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Subcentimeter pulmonary nodules are frequently detected on computed tomographic (CT) scans of the chest in smokers, and some of these nodules are almost certainly early lung cancers. However, subcentimeter pulmonary nodules cannot be reliably biopsied percutaneously [1, 2]. Thoracoscopic surgical excision of small pulmonary nodules or of somewhat larger ill-defined lesions is limited by the frequent inability to see, palpate, or instrumentally locate these lesions [3]. This results in conversion to an open thoracotomy or the thoracoscopic removal of a large amount of lung tissue in the hope of incorporating the lesion in the surgical specimen. Both of these maneuvers may result in an increase in morbidity and potential mortality for the patient. It remains an open question whether very early detection and excision of lung cancer will improve survival. However, this question cannot be answered until a reliable method for the excision of small lung nodules is developed.

Several lung nodule localization techniques have been previously reported to facilitate the successful thoracoscopic localization and excision of the above-described lesions. These include CT-guided methylene blue pleural localization [4, 5], preoperative percutaneously placed hooks of various design [6–8], tomographic-guided preoperative bronchoscopically placed barium markers with subsequent intraoperative fluoroscopically guided biopsy [9], preoperative CT-guided percutaneous placement of cyanoacrylate with subsequent intraoperative fluoroscopic-guided biopsy [10], and preoperative CT-guided placement of radioopaque Lipiodol (Mitsui Pharmaceutical Co, Tokyo, Japan) with subsequent fluoroscopic-guided biopsy [11, 12]. Chella [13] has described the preoperative percutaneous placement of a technetium radiotracer in or near the lung lesion using CT fluoroscopic guidance with subsequent thoracoscopic localization using an endoscopic radioprobe. Burdine [14] and Sugi [15] have described similar radiotracer localization techniques using different radiotracer solutions. The radiotracer solutions used by these three investigators are either unavailable routinely in North America or dissipated from the localization site too quickly to allow practical coordination with the subsequent surgical procedure.

The purpose of this work was to develop a reliable technique for the localization of small lung nodules and subsequent thoracoscopic excisional biopsy. The present study was composed of two parts. First we evaluated three readily available radiotracer solutions in a labora''tory animal lung to determine which had the most precise and sustained localization area over time. Next, using the radiotracer that tested best in the laboratory study, we performed CT-guided radiotracer injection for nodule localization with subsequent thoracoscopic excision of small or ill-defined lesions in patients felt to be at risk for a primary lung cancer. The results from the first 13 patients treated at our institution are presented and discussed.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
Part 1: radiotracer dynamics in the rat lung
This component of the study was performed using a dual modality small animal scanner developed by Mark B. Williams, PhD, at the University of Virginia. The scanner consists of a digital radiography system integrated with a gamma camera so the roentgenogram transmission and gamma ray emission images may be obtained in rapid sequence, and automatically coregistered and fused. Using the digital radiographic portion of the system, the right lung of 12 male Sprague-Dawley rats was injected transthoracically under roentgenogram guidance with 0.06 mL of a technetium 99m (Tc 99m) radiotracer solution: 4 each with macroaggregated albumin (MAA), unfiltered sulfur colloid (SC), and pertechnetate (TcO4). The injected activity ranged from 75 to 200 µCi. Animals were anesthetized with ketamine 60 mg/kg and xylazine 6 mg/kg IP. Anterior-posterior and lateral scans obtained 1 minute postinjection were used to confirm intraparenchymal lung injection.

Sequential coregistered anterior-posterior radiographs and scintigrams of the chest and abdomen were obtained at 1 minute, 30 minutes, and then 1, 2, 3, and 4 hours postinjection (Fig 1). Each scintigram was analyzed as follows. A region of interest (ROI) was drawn containing the lungs. To measure the area of the injection site, pixels within the lung having counts more than 10% of peak count in the image were identified, and these pixels were considered to be the injection site. The injection site area was determined by summing the area of these pixels. Decay corrected activity within the injection site was measured at the 30 minutes, and then 1, 2, 3, and 4 hours postinjection time points. This study was approved by our institutional animal care review board, and all animals received humane care in accordance with the Guide for the Care and Use of Laboratory Animals published by the National Institutes of Health (National Institutes of Health publication 85 to 23, revised 1985).



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  		Fig 1. Combined radiographs and scintigrams obtained 1 minute and 4 hours after the injection of radiotracer into the right lung of a Sprague-Dawley rat. Three rats are illustrated: one each injected with technetium 99m (Tc 99m) macroaggregated albumin (MAA), sulfur colloid, or pertechnetate (TcO4). Note the injection site diameter was the smallest for MAA and did not change appreciably after 4 hours for either MAA or sulfur colloid. For TcO4, no residual activity was seen in the injection site after 4 hours and significant uptake in gastric mucosa was also seen. It is well known that intravenous TcO4 is concentrated by gastric mucosa as demonstrated by uptake in the ectopic gastric mucosa of a Meckle's diverticulum during a Meckle's scan.

 
Part 2: radiotracer lung nodule localization in human patients
A retrospective review of the first 13 patients to undergo radiotracer lung nodule localization with subsequent thoracoscopic biopsy, performed at our institution, was studied following approval by our institutional IRB (protocol approval date: June 2003). All patients were referred for the evaluation of a suspicious lung nodule (Figs 2A and 2B). Patient selection was based on the clinical assessment of the anticipated difficulty in thoracoscopically locating the nodule. This assessment included either the nodule size, its ground glass appearance, its depth from the parietal pleural surface, or a combination of these factors. Patient selection was also based on the clinical risk of developing lung cancer as expressed in age and smoking history. The patient demographics are depicted in Table 1. There were 9 male and 4 female patients with a mean age of 59.2 years old. Twelve of 13 patients were current or former smokers. All of the nodules were initially diagnosed by CT scan. The CT scans were performed for lung cancer screening or the lung nodules were discovered as incidental findings on CT scans done for other purposes. Percutaneous biopsy was attempted in one patient before the lung nodule localization procedure but insufficient tissue was obtained.



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  		Fig 2. Computed tomographic (CT) images depicting appearance of biopsy proving (A) bronchioloalveolar cell carcinomas adenocarcinoma (patient 1) and (B) a benign nodule (patient 7) are similar, which demonstrates that, for small lung nodules, benign and malignant lesions cannot be reliably distinguished on CT. Needle tip abutting nodule (B) is illustrated immediately before the injection of 99mTc (C) MAA. (MAA = macroaggregated albumin.)

 

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  		Table 1. Patient Data

 
On the morning of surgery, all patients, after conscious sedation, underwent a limited chest CT without intravenous contrast to identify the nodule. Using fluoroscopic CT guidance, a 22-gauge spinal needle was advanced into or immediately adjacent to the lung nodule and 0.1 mL of Tc 99m MAA (approximately 0.3 mCi) was injected (Fig 2C). Four different radiologists performed the procedure in the 13 patients. Following the procedure, patients recovered from conscious sedation in the radiology department for approximately 1 hour, and then reported to surgical admitting.

All patients subsequently underwent general anesthesia with single lung ventilation of the contralateral lung. Patients were placed in the lateral decubitus position. Three small thoracoscopic incisions were made: one for a 10-mm diameter 30-degree telescope, one for an endoscopic grasper, and one for dual use to insert a sterile gamma probe and an endoscopic stapler for subsequent lung resection.

All procedures involved the following sequence. After endoscopic visualization of the lung surface, a gamma radioprobe (C-Trak; Care Wise Medical Products Corp., Morgan Hill, CA) was inserted and radioactivity in counts per second (CPS) was determined over the general area where the lesion was believed to be. This was based on the CT scan and the information supplied by the site of the needle insertion in the chest wall. The lung surface exhibiting maximum radioactivity was then grasped by an endoscopic forceps. The probe then more precisely queried the area under the grasper to determine the maximum signal source using different probe angles. Early in the study a straight (0 degree) endoscopic gamma probe was used. The collimator aperture had a diameter of 10 mm and the overall probe length was 47 cm. Subsequently, a 37-cm long thoracic probe with a 30-degree bend in it was used. For this probe, the collimator aperture size was 15 mm. Following localization, the probe was removed and replaced by an articulating endostapler for excisional biopsy of the area of maximum radioactive signal.

Frozen section pathologic examination of all specimens was performed intraoperatively to make a diagnosis and confirm the removal of a lesion conforming to the CT abnormality. All patients found to have primary lung cancers underwent immediate lobectomies and nodal staging by muscle-sparing vertical axillary incisions.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Part 1: radiotracer dynamics in the rat lung
Injection of radiotracer in the right lower lung was confirmed on imaging for all 12 animals (Fig 1). Averaging the data for the four rats injected with each radiotracer, the mean areas of the initial injection sites were 74.5 ± 47.5, 157.1 ± 60.8, 133.7 ± 39.4 mm2 for MAA, SC, and TcO4, respectively. The initial injection site area was smallest for MAA and largest for SC. In all 4 animals that received TcO4, the radiotracer was rapidly cleared from the injection site and uptake by the gastric mucosa was seen (Fig 1). After 4 hours, more than 80% of the initial MAA and SC decay-corrected activity remained in the initial injection site. Thus, the mean injection site area for MAA and SC remained essentially constant more than 4 hours.

Part 2: radiotracer lung nodule localization in human patients
All 13 patients undergoing preoperative radiotracer marking of their solitary lung nodule or ill-defined mass had their lesions successfully localized (Table 1). In several patients the radiotracer allowed rapid identification of the approximate nodule location. This was followed by instrumental or digital palpation to confirm the exact localization of the nodule before excisional biopsy. All resection margins were microscopically clear. In 1 patient (patient 7), a dense pleurodesis required abandonment of the thoracoscopic approach. An open thoracotomy was done and the small nonpalpable nodule was localized by the radioprobe and successfully excised. In another patient (patient 12), the lesion was located 3.5-cm deep in the lobe and adjacent to major bronchovascular hilar structures and was successfully localized with the radioprobe. Thoracoscopic excision was attempted but abandoned due to the inability of the endoscopic stapling device to perform deep biopsies. Conversion to an open thoracotomy led to successful excisional biopsy. All other nodules in patients were localized using the radioprobe and successful thoracoscopic excisional biopsy was performed.

The range of time from the radiotracer injection to the initial surgical skin incision was 76 minutes to 8.1 hours with a mean time of 186 minutes. Use of the Tc 99m MAA radiotracer in humans confirmed the animal laboratory finding of maintenance of a small localized injection site size for up to 8 hours. Because surgical case start times are often unpredictable, the stability of the radiotracer in vivo after CT-guided placement greatly enhanced its adaptation to the operating suite realities.

Lesion characteristics in the study were as follows. The average distance from the chest wall pleural surface to the outer edge of the lesion on CT was 12.7 mm with a range of 1 to 47 mm. CT morphologic characteristics were 7 solid lesions, 4 ground-glass, and 2 mixed solid and ground-glass. Lesion size on pathologic description ranged from 4 to 23 mm with a median size of 10 mm. Seven of 13 lesions were malignant. Five of these were primary lung cancers, all of which were stage IA adenocarcinomas or bronchioloalveolar cell carcinomas (BAC). Two were solitary metastatic nodules (melanoma and renal cell) in patients who had a history of previous extrathoracic malignancies and who also had significant smoking histories. The average age of all patients was 59 years old with a range of 48 to 77 years old. The average age of the patients found to have primary lung cancers was 64.8 years old with a range of 52 to 77 years old.

There were no complications related to the radiotracer localization procedure, and there were no surgical complications. The average length of stay (LOS) for patients undergoing wedge excision was 2 days (range 1 to 4 days). The average LOS for patients undergoing biopsy and subsequent lobectomy was 3.9 days (range 3 to 4 days).


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Previously described techniques for thoracoscopic localization of small lung nodules have each had features that limit their clinical application. Wicky [4], Partrick [5], and Lenglinger [16] reported on the efficacy of CT-guided methylene blue injection of the pleura over the underlying nodule. We have found the dye frequently dissipates over a large area by the time the surgical procedure is done, making its localization features inadequate. In addition, it does not denote the depth of the lesion and therefore offers no guide to the required depth of the excisional biopsy for lesions greater than 1 cm below the pleural surface. Attempts to use percutaneously placed Kopans needles or other hooked devices [6, 7] have, in our clinical experience, been unreliable due to the frequent failure of the device to stay in the region of the nodule. Partik [8] has recently described a helical tip wire specially designed for lung localization. This technique requires an 18-gauge needle introducer and was associated with a 31% incidence of pneumothorax. Another disadvantage of needle localization is the fact that the surgeon's view of the lung is often from a different angle than that of the radiologist placing the needle [14]. Tracking the wire down to the lesion may be difficult to do if it is not in the exact plane that the thoracoscope views. In addition, as pointed out by Partik [8], the wire may cross a fissure on its way to the nodule making thoracoscopic resection more difficult.

Bronchoscopic placement of a barium marker has been described by Okumura [9] with subsequent intraoperative use of fluoroscopy to locate the radioopaque substance placed near the lung nodule. The bronchoscopic skill required to do such localization is not readily available at most institutions. In addition, the requirement for fluoroscopy in the operating room and the limited viewing angles available with a patient in the lateral decubitus position make this technique cumbersome.

Localization involving CT-fluoroscopic injection of Lipiodol into or near the nodule has been described by Nomori [12]. Successful localization and excision was achieved in all patients, but possible systemic embolization of the marking solution and intraoperative need for fluoroscopy limit this technique's usefulness.

Transthoracic placement of a cyanoacrylate material using CT guidance was reported by Yoshida [10]. A firm, readily visible mass was readily found at thoracoscopy. However, two serious limitations were noted: the hardness of the localization material made pathologic sectioning for examination of the specimen difficult; the concern about possible embolization of the material into the systemic circulation.

Computed tomographic guided placement of a radiotracer for lung nodule localization was first described by Chella [13]. All 39 patients underwent successful localization using a solution of Tc 99m-labeled human serum albumin microspheres. However, this radiotracer is not available in the United States. Burdine [14] subsequently reported a radiotracer localization technique using unfiltered Tc 99m sulfur colloid, which is the same substance used for breast sentinel node detection. Loss of signal was an apparent problem with this radiotracer in the lung environment because patients were "transported immediately to the operating room" with an average time between CT injection and operating room localization of 67 minutes. Burdine's technique thus requires immediate access to the surgical suite, which is a significant limitation in most institutions. Sugi [15] described the successful use of Tc 99m tin colloid and Tc 99m phytate to guide thoracoscopic biopsy of lesions averaging 13.8 mm in size. Neither the tin colloid nor phytate suspension are available in the U.S. However, they successfully localized small pulmonary nodules in 25 patients without complication from the radiology procedure or surgery. The injected dose ranged from 2 to 4 mCi, approximately 10 times the dose used in our study. Sugi [15] used special radiation precautions in the handling of the surgical specimens. The injected dose in our study, 0.3 mCi, is slightly less than typically used for sentinel lymph node mapping. No special radiation protection precautions in the operating room or in handling the surgical specimens are thought to be required for sentinel lymph node mapping and, thus, none were used in the current study of lung nodules.

The results of our animal study suggest that either Tc 99m-labeled MAA or SC could be used for radiotracer-guided lung nodule localization, and both demonstrated good retention in the rat lung for 4 hours following direct intraparenchymal injection. The Tc 99m-labeled MAA had a smaller injection site diameter, which may provide more precise localization and permit smaller wedge resections. The particle size of Tc 99m-labeled MAA is more than 10 times greater than Tc 99m-labeled SC. This large particle size may impede particle diffusion within the lung and may contribute to the smaller injection site diameter of Tc 99m-labeled MAA.

The results of our feasibility study in humans using a solution of Tc 99m-labeled MAA revealed the following advantages when compared to previous techniques. Because no needle is left in place, dislodgement and trans-fissural positioning cannot occur. The substance used is readily available. Because it is routinely injected intravascularly to perform lung perfusion scans the risk of radiotracer embolization is associated with neglible morbidity. The procedure for Tc 99m MAA placement requires skill with CT-guided injection that is readily available in most institutions. The injection requires much less of a radiologist's time than attempts to aspirate diagnostic material from these small lung nodules. The procedure does not require intraoperative fluoroscopy, but can be done with a gamma probe available in any operating unit that performs sentinel node surgery. The endoscopic straight probe or the thorascopic 30-degree probe provide additional flexibility for thoracoscopic procedures. Frozen and permanent pathologic examination of the specimen are not affected by the localization technique and there is no significant risk to operating room and pathology department personnel from the low-dose gamma radiation. Our laboratory studies suggested (and our subsequent clinical experience has confirmed) that Tc 99m-labeled MAA produces a small intraparenchymal injection site that maximizes accuracy of lung nodule localization while minimizing tissue removed for the biopsy. Our animal data and clinical experience demonstrate that Tc 99m MAA is quite stable in the lung for up to 8 hours.

Our study did indicate some limitations. The biggest limitation remains that of the inherent difficulty in coordinating an operation with any preoperative same-day procedure. It is conceivable that radiotracer placement the evening before surgery might demonstrate enough sustained activity the following day to permit radiotracer guided thoracoscopic biopsy. Any thoracoscopic procedure is handicapped by the intraoperative discovery of a dense pleurodesis. In the one patient in our study that required conversion to an open thoracotomy because of a pleurodesis, the presence of the radiotracer still helped in the subsequent intraoperative localization of the small, nonpalpable nodule. In one other patient in the present study that required conversion to an open thoracotomy for biopsy is instructive in that the lesion was well-localized by the radiotracer marker but it lay deep and adjacent to peribronchial structures where thoracoscopic instruments could not successfully be used to excise it.

In summary, preoperative radiotracer lung nodule localization is feasible and a promising technique for assisting excisional diagnostic biopsy of possible early lung cancer presenting as a small pulmonary nodule or an ill-defined lesion. If further clinical use of this technique confirms its reliability and low morbidity and mortality, then, as discussed by Ost and coworkers [17] in a recent clinical practices review, "the strategy of proceeding directly to video-assisted thoracoscopic surgery becomes more effective than other diagnostic approaches" for the management of solitary pulmonary nodules.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
Thanks to Julia Zaporozhan, BS, and Bijoy Kundu, PhD, for data collection and analysis, to the following radiologists who performed the lung nodule localization procedures: Spencer B. Gay, MD, Juan Olazagasti, MD, Matthew Bassignani, MD, and Jonathan Ciambotti, MD, and to the following cardiothoracic fellows who participated in the operations: Jay Gangemi, MD, Josh Rovin, MD, Jason Sperling, MD, and Trip Zorn, MD.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Tsukada H., Satou T., Iwashima A., Souma T. Diagnostic accuracy of CT-guided automated needle biopsy of lung nodules. AJR Am J Roentgenol 2000;175:239-243.[Abstract/Free Full Text]
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  4. Wicky S., Mayor B., Cuttat J.F., et al. CT-guided localization of pulmonary nodules with methylene blue injections for thoracoscopic resections. Chest 1994;106:1326-1328.[Abstract/Free Full Text]
  5. Partrick D.A., Bensard D.D., Teitelbaum D.H., et al. Successful thoracoscopic lung biopsy in children utilizing preoperative CT-guided localization. J Pediatr Surg 2002;37:970-973.[Medline]
  6. Paci M., Annessi V., Giovanardi F., et al. Preoperative localization of indeterminate pulmonary nodules before videothoracoscopic resection. Surg Endosc 2002;16:509-511.[Medline]
  7. Saito H., Minamiya Y., Matsuzaki I., et al. Indication for preoperative localization of small peripheral pulmonary nodules in thoracoscopic surgery. J Thorac Cardiovasc Surg 2002;124:1198-1202.[Abstract/Free Full Text]
  8. Partik B.L., Leung A.N., Mller M.R., et al. Using a dedicated lung-marker system for localization of pulmonary nodules before thoracoscopic surgery. AJR Am J Roentgenol 2003;180:805-809.[Abstract/Free Full Text]
  9. Okumura T., Kondo H., Suzuki K., et al. Fluoroscopy-assisted thoracoscopic surgery after computer tomography-guided bronchoscopic barium marking. Ann Thorac Surg 2001;71:439-442.[Abstract/Free Full Text]
  10. Yoshida J., Nagai K., Nishimura M., et al. Computed tomography-fluoroscopy guided injection of cyanoacrylate to mark a pulmonary nodule for thoracoscopic resection. Jpn J Thorac Cardiovasc Surg 1999;47:210-213.[Medline]
  11. Moon S.-W., Wang Y.-P., Jo K.-H., et al. Fluoroscopy-aided thoracoscopic resection of pulmonary nodule localized with contrast media. Ann Thorac Surg 1999;68:1815-1820.[Abstract/Free Full Text]
  12. Nomori H., Horio H., Naruke T., et al. Fluoroscopy-assisted thoracoscopic resection of lung nodules marked with lipiodol. Ann Thorac Surg 2002;74:170-173.[Abstract/Free Full Text]
  13. Chella A., Lucchi M., Ambrogi M.C., et al. A pilot study of the role of Tc-99 radionuclide in localization of pulmonary nodular lesions for thoracoscopic resection. Eur J Cardiothorac Surg 2000;18:17-21.[Abstract/Free Full Text]
  14. Burdine J., Joyce L.D., Plunkett M.B., Inampudi S., Kaye M.G., Dunn D.H. Feasibility and value of video-assisted thoracoscopic surgery wedge excision of small pulmonary nodules in patients with malignancy. Chest 2002;122:1467-1470.[Abstract/Free Full Text]
  15. Sugi K., Kaneda Y., Hirasawa K., Kunitani N. Radioisotope marking under CT guidance and localization using a handheld gamma probe for small or indistinct pulmonary lesions. Chest 2003;124:155-158.[Abstract/Free Full Text]
  16. Lenglinger F.X., Schwarz C.D., Artmann W. Localization of pulmonary nodules before thoracoscopic surgery: value of percutaneous staining with methylene blue. AJR Am J Roentgenol 1994;163:297-300.[Abstract/Free Full Text]
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