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Ann Thorac Surg 2006;82:1191-1197
© 2006 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Clinical Experience With Radiotracer-Guided Thoracoscopic Biopsy of Small, Indeterminate Lung Nodules

Brendon M. Stiles, MDa, Talissa A. Altes, MDb, David R. Jones, MDa, K. Robert Shen, MDa, Gorav Ailawadi, MDa, Spencer B. Gay, MDb, Juan Olazagasti, MDb, Patrice K. Rehm, MDb, Thomas M. Daniel, MDa,*

a Department of Surgery, University of Virginia Health System, Charlottesville, Virginia
b Department of Radiology, University of Virginia Health System, Charlottesville, Virginia

Accepted for publication April 20, 2006.

* Address correspondence to Dr Daniel, Department of Surgery, Box 800679, University of Virginia Health System, Charlottesville, VA 22908-0679 (Email: tmd5m{at}virginia.edu).

Presented at the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 30–Feb 1, 2006.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: Although computed tomography lung-screening programs report a 31% to 51% incidence of subcentimeter pulmonary nodules, 85% are too small to biopsy or interrogate with positron emission spectroscopy scans. We developed a technique using transthoracic percutaneous radiotracer injection with thoracoscopic radioprobe localization and excision for small pulmonary nodules. This report describes our series of the first 46 patients evaluated with this technique.

METHODS: Forty-six patients (79% smokers; 52% males; median age, 64 years) were evaluated. Patient selection was based on the surgeon's anticipated difficulty in thoracoscopically locating small nodules because of lesion size or location. Computed tomographic-guided injection of radiotracer solution was made into or adjacent to the nodule the day of surgery. Intraoperative gamma probe localization, followed by thoracoscopic excision of the lesion, was subsequently performed.

RESULTS: Median nodule size was 9 mm (range, 3 to 22 mm), and median depth was 5 mm (range, 0 to 50 mm). Forty-four (96%) of the lesions were successfully localized and excised. Median time from injection to surgery was 270 minutes. Failures were the result of inadvertent pleural or chest wall radiotracer placement. Forty-six percent (21 of 46) of the lesions were malignant, of which 71% (15 of 21) were primary lung cancers. Patients with lung cancer underwent lobectomy or segmentectomy. Fourteen of 15 were stage IA, whereas 1 was stage IIIB (6 mm primary with 4 mm intralobar metastasis). Complications were three pneumothoraces at the time of radiotracer injection.

CONCLUSIONS: Computed tomography-guided radiotracer localization of small pulmonary nodules combined with thoracoscopic excisional biopsy is feasible and safe. This technique successfully localized and excised the nodule in 96% of cases.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 References
 
The increased use of chest computed tomography (CT) in lung cancer screening programs and for various clinical applications has led to identification of significant numbers of indeterminate lung nodules. Improved CT technology allows diagnosis of not only more nodules, but also increasingly smaller nodules [1, 2]. Thoracic surgeons are now being called on to evaluate these lesions for the possibility of malignancy, often in the setting of high-risk patients with significant smoking histories. Although short-term follow-up imaging may often suggest either benignity or malignancy, caution should be exercised in accepting a benign diagnosis without tissue confirmation. Additionally, given evidence that tumor size directly impacts survival even within subgroups of stage IA tumors, it makes intuitive sense to attempt to treat potential cancers as early as possible [3–5].

We and others have found that small lung nodules, particularly subcentimeter nodules, cannot be reliably biopsied percutaneously [6, 7]. A recent report also suggested that percutaneous needle biopsy of small cancers (stage I) is associated with a significantly increased risk of pleural recurrence [8]. Because of these potential problems, surgical excisional biopsy of these small, indeterminate pulmonary nodules is often performed at our institution. Thoracoscopic surgery carries less morbidity than diagnostic procedures performed through thoracotomy, but is limited by the frequent inability to see or palpate (digitally or instrumentally) small subpleural lesions [9–12]. To overcome this limitation, several different thoracoscopic nodule localization techniques have been developed and have been reported to improve the ease and accuracy of thoracoscopic biopsy. These include the use of visual markers, such as methylene blue and hook wires, fluoroscopic localization using various radiopaque markers, radiotracer localization techniques, and more recently, thoracic endosonography [13–25]. All of these techniques have their own advantages and disadvantages, as well as significant learning curves.

At our institution, CT-guided radiotracer injection followed by intraoperative thoracoscopic radioprobe localization is the preferred method for finding nodules that we anticipate preoperatively will be difficult to see or palpate. We have previously reported on the radiotracer dynamics in an animal model and on our first use of this technique in human patients [26]. In this study, we describe consecutive patients with small, solitary, indeterminate lung nodules in which we used radiotracer localization. It is our intent to show that this technique is safe and effective and that it facilitates the diagnosis of a significant number of early stage lung cancers.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 References
 
Patients
Our institutional review board reviewed our proposal to place technetium radionuclide to guide subsequent lung biopsy. They determined that this technique had been documented in the medical literature by two groups and that it did not need institutional review board approval [24, 25]. All patients were informed of the procedure's benefits, risks, and limitations and gave their written approval. Subsequent approval for retrospective chart review was also obtained from our institutional review board. Between November 2002 and July 2005, 46 patients underwent radiotracer injection followed by thoracoscopic localization for solitary indeterminate nodules. The portal of entry into our study was a thoracic surgery consult. All patients had been referred by pulmonologists or primary care physicians and were thought to be at risk for the development of lung cancer. Patients were selected for the radiotracer procedure when there was anticipated difficulty in thoracoscopically locating their nodules. This assessment, made by the thoracic surgeon, was based on nodule size, depth, location, and appearance. Of the patients selected, 55% were male and 79% had a smoking history (28% current smokers). The median age of the group was 64 years with a range from 34 to 80 years. Eleven patients had positron emission spectroscopy scans as part of their workup, of which 7 had a positive result.

Technique
On the morning of surgery, under conscious sedation, all patients underwent a limited chest CT without contrast to confirm nodule location. The operating surgeon and CT radiologist mutually decided on the exact lung site to be marked and on the best approach angle for radiotracer placement. After confirmation, a 20-guage coaxial needle was positioned in the chest wall just proximal to the pleural cavity. A 22-gauge spinal needle was then advanced through this needle into or adjacent to the lung nodule under CT fluoroscopy. Once properly positioned, 0.1 mL of technetium Tc 99m macro-aggregated albumin (Tc 99m MAA; approximately 0.3 mCi) was injected. We routinely obtained an immediate postprocedure scintigram to confirm intraparenchymal location of the radiotracer. The patient then recovered from conscious sedation, reported to surgical admitting, and was subsequently taken to the operating room when a room was available.

General anesthesia with single-lung ventilation was induced. Once adequately prepped and draped, a 37-cm-long sterile gamma radioprobe with an angled head (C-Trak; Care Wise Medical Products Corp, Morgan Hill, CA) was used to first locate the area of maximum intensity on the chest wall. This helped to plan subsequent thoracoscopic port sites. Three incisions were then made: one for a 5-mm 30-degree thoracoscope, one for an endoscopic grasper, and one for the gamma probe and Endostapler used sequentially. The area of the lung parenchyma with maximum radioactive signal was grasped and elevated with the endoscopic grasper, and the radioprobe was used to confirm the lesion's location from multiple angles. The radioprobe was reintroduced as often as necessary during the stapling process to assure that the lung tissue that was excised contained the maximum radioactive signal. The lesion was wedged out with the Endostapler, and the specimen was removed in an endobag. Once the lesion was removed, the radioprobe was used to confirm absence of signal in the remaining lung and to determine scintigram counts of the resected specimen. The site of maximum activity in the specimen was marked with a suture for pathologic localization. The tissue samples were sent for frozen-section pathologic examination. Patients found to have primary lung cancers underwent immediate thoracotomy with lobectomy or segmentectomy and nodal staging.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 References
 
Nodule Characteristics and Technical Aspects
Forty-six patients with indeterminate pulmonary nodules had radiotracer placement and attempted thoracoscopic localization and resection, with a lobar distribution as follows: 8 left lower lobe, 8 left upper lobe, 16 right lower lobe, 5 right middle lobe, and 9 right upper lobe. For all 46 patients, the median nodule size was 9.0 mm (range, 3 to 22 mm), and median depth from the pleural surface was 5 mm (range, 0 to 50 mm). Nodules at the pleural surface (0 mm depth) were selected based on location or appearance and anticipated difficulty of thoracoscopic localization (Fig 1). These nodules usually lay in subpleural locations not reachable by digital palpation, such as the apical, diaphragmatic, or mediastinal pleural regions. All radiotracer injections were confirmed with scintigraphy (Fig 2). Three patients experienced small pneumothoraces as a result of the injection procedure. All of these were managed conservatively and none required chest tube placement before surgery. Median time from injection of the radiotracer solution to the beginning of surgery was 270 minutes, with a maximum time of 720 minutes (patient was delayed for an emergent case). The reduction of radioactive signal related to the 6-hour half-life of Tc 99m MAA in the delayed cases did not affect our ability to localize the lesions.


Figure 1
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  		Fig 1. Patient selection for radiotracer localization was based on anticipated difficulty in thoracoscopically locating nodules with visualization and palpation alone. Some patients were selected on the basis of the depth of the nodule (A), whereas others were selected on the basis of the location of the lesion. The lesion seen in (B) was judged to be pleural based, but was abutting the mediastinum.

 

Figure 2
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  		Fig 2. After computed tomographic–guided technetium Tc 99m macro-aggregated albumin injection into or near the nodule, an immediate postprocedure scintigram is obtained to confirm intraparenchymal location of the radiotracer. The left panel shows a lateral view of the patient's scintigram with the radiotracer appearing as a white spot in the superior segment of the right lower lobe where the nodule was marked by the technetium/albumin injection. The right panel shows the anterior-posterior view of the same patient with the marker in the superior segment of the right lower lobe.

 
Radioprobe localization and thoracoscopic excision was possible in 96% (44 of 46) of patients. The two failures were the result of radiotracer spillage into the pleural space. Both events were recognized preoperatively (Fig 3). This caused a diffuse radioactive signal within the pleural cavity that made thoracoscopic localization impossible. The lesions were successfully located by digital palpation after converting to open thoracotomy. Forty-six percent (21 of 46) of the resected nodules were malignant by frozen-section analysis (Table 1). Of these, 15 were primary non–small cell lung cancer (NSCLC), 5 were metastases from non–lung primaries, and 1 was a lymphoma. Of the 7 patients who had positive preoperative positron emission spectroscopy scans, 5 had malignancies (4 NSCLCs, 1 metastatic) and 2 were positron emission spectroscopy–avid benign lesions. One patient with metastatic cancer had a false-negative positron emission spectroscopy scan. The 15 patients who had NSCLC all underwent thoracotomy and anatomic excision of their cancers (14 lobectomies, 1 segmentectomy). Median length of stay was 4 days (range, 3 to 5 days) for the NSCLC patients, but only 1 day for the patients who underwent the thoracoscopic localization and excision procedure only (range, 0 to 6 days). There were no postoperative complications other than urinary retention in 1 patient, which required outpatient catheterization.


Figure 3
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  		Fig 3. We successfully localized 96% (44 of 46) of the lesions in our series. The two failures were related to radiotracer spillage into the pleural cavity, which was recognized preoperatively. In this scintigram, the lesion is marked with an arrowhead, and the spilled tracer is denoted with an arrow. Placement of the radiotracer deep to subpleural lesions minimizes the chances of inadvertent pleural space injection.

 

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  		Table 1. Findings at Pathologic Examination
 
Characteristics of Nodules Found To Be Non–Small Cell Lung Cancer
Subgroup analysis was performed on the patients found to have NSCLC by pathologic examination (Table 2). Median nodule size was 9 mm (range, 6 to 22 mm). Sixty-seven percent (10 of 15) of the nodules were less than or equal to 1 cm. Median nodule depth was 5 mm (range, 0 to 50 mm). On pathologic analysis, 93% (14 of 15) were found to be stage IA tumors. The only tumor not found to be stage IA was a 6-mm adenocarcinoma in which a second 4-mm focus of adenocarcinoma was interpreted as an intralobar metastasis, thus upstaging the tumor to stage IIIB. These lesions could well be considered two separate stage IA primaries. The finding does justify our policy of performing an accepted oncologic resection until such time as it can be demonstrated that lesser resections provide equivalent outcomes. The majority of patients had adenocarcinoma (11 of 15), whereas the remainder had squamous cell (3) or large cell (1) tumors. Seven of the nodules were located 22 to 50 cm deep from the pleural surface. All were successfully localized by the technique, and six were excised thoracoscopically. The seventh lesion was 5 cm deep, and attempted thoracoscopic excision was converted to an open excision when radioprobe localization showed the lesion to lie closer to major bronchovascular structures than had been anticipated preoperatively.


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  		Table 2. Characteristics of Patients and Nodules With Non–Small Cell Lung Cancer
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 References
 
The management of small, indeterminate pulmonary nodules is a challenging problem that thoracic surgeons are now encountering more frequently. Ever-smaller nodules are being detected with improvements in CT technology [1, 2]. Henschke's group [27] has suggested that such nodules, particularly those less than 5 mm, can be followed safely with serial CT scans to assess for growth. Such nodules are said to be unlikely to be malignant. However, there is a much greater rate of malignancy in nodules greater than 5 mm. Of the first 1,000 patients screened in the Early Lung Cancer Action Project, 94 patients had nodules between 5.0 and 9.0 mm. As previously reported, 10 of 84 of these patients (12%) were diagnosed with malignancy with follow-up [27]. The risk of malignancy in nodules greater than 10 mm is even higher and has been well established.

Although it is intuitive that excision of smaller tumors leads to treatment at an earlier stage and to improved survival, this has only recently been demonstrated conclusively [5, 28, 29]. Given these data, it is essential to definitively establish a diagnosis for small lung nodules in high-risk patients. We have not found percutaneous biopsy to be useful for these lesions, particularly for subcentimeter nodules. Others have reported a significant risk of false-negative results and complications with this technique [30, 31]. Positron emission spectroscopy scans have not been shown to be reliable for subcentimeter nodules and may give false-negative results for carcinoid tumors and bronchoalveolar carcinomas [32, 33].

Surgical excisional biopsy is the most accurate means toward obtaining a definitive tissue diagnosis for suspicious, small nodules. Thoracoscopy unfortunately is often limited by the inability to see or digitally palpate the lesion within the lung parenchyma [9–12]. Suzuki and associates [9] reported a 54% conversion rate to thoracotomy when using visualization and digital palpation only to localize small nodules. This conversion rate increased to 63% for subcentimeter nodules. To that end, several small nodule localization techniques have been developed and described in the literature in an attempt to improve the accuracy of thoracoscopic resection [13–25]. The most commonly used techniques include percutaneous placement of dye, hooks, or coils, placement of radiopaque markers with subsequent fluoroscopic localization, and the use of intraoperative ultrasonography. Dye placement is limited by diffusion away from the nodule and difficulty in visualization in patients with extensive anthracotic pigmentation. Placement of hooks or coils has a high incidence of dislodgement and may be associated with pneumothorax, intrapulmonary hemorrhage, or air embolism [34–36]. In our experience, dislodgement is particularly likely to happen when marking subcentimeter lesions, as the hook will not be radiologically in the substance of the lesion but rather in the adjacent lung parenchyma in which there is minimal resistance. Another major disadvantage with wire localization techniques is the fact that the surgeon has to follow the plane of the wire to biopsy the lesion. This works well for lesions adjacent to the chest wall but does not work well when the wire crosses extensive lung tissue to localize a lesion in areas of the lung at varying depths beneath the apical, diaphragmatic, or mediastinal surfaces of the lung. Radiotracer localization frees the surgeon to approach the lesion by the shortest distance from the pleural surface.

Intraoperative ultrasound is appealing in that it requires no preoperative coordination with another specialty. However, intraoperative localization of subcentimeter lesions in partially air-filled lungs is extremely difficult and requires expertise in ultrasonography that is acquired only after extensive experience. This technique is also particularly difficult and time-consuming in patients with emphysematous lungs that are difficult to completely collapse [21–23]. Cyanoacrylate localization is a focal technique, but it requires intraoperative fluoroscopy with its attendant risks to the patient and the entire operative team [17]. Another major drawback is the fact that frozen pathologic study for immediate intraoperative decisions is not possible because of the inability of the pathologist to cut through the firm localizing material to obtain a specimen. Soft radiopaque materials such as Lipiodol do not have this disadvantage but do require intraoperative fluoroscopy with its attendant risks and physical limitations when examining the atelectatic lung in the lateral decubitus position [18, 19].

We chose to perform CT-guided radiotracer injection using a Tc 99m MAA solution, followed by intraoperative thoracoscopic localization with a gamma probe, because it allowed marking of lesions anywhere in the lung up to 5 cm deep from the pleura. This technique does not require intraoperative fluoroscopy, does not require a skilled ultrasonographer, and uses an available radionuclide (lung scan), available radioprobes (breast sentinel node procedures), available CT technology, and available thoracoscopic technology. The radioisotope dose required for our technique (0.3 mCi) is only one third the dose of the same isotope used in breast lymphoscintigraphy (1 mCi) and much less than that used for lung scans (4 to 5 mCi) and bone scans (10 to 20 mCi). Like all procedures that require CT-guided placement of dyes, hooks, or radiotracer, there is also some risk of pneumothorax. In the few case in which this happened, pigtail catheter placement allowed the patient to proceed to surgery without further problems.

We have found the radiotracer localization technique to be safe and effective, as evidenced by our low overall morbidity (8.7%) and mortality (0%) rates, our short length of stay (median, 1 day for patients without NSCLC), and our high rate of malignancy in resected nodules (46%). Radiotracer techniques are applicable to large areas of the lung. Our series included nodules in all five lobes at depths up to 5 cm and in areas adjacent to the mediastinum, the diaphragm, and the lung apices. We believe that we have overcome the problem of radiotracer diffusion with the Tc 99m MAA solution. It has a small intraparenchymal injection site diameter and does not dissipate rapidly into the lymphatic system or surrounding parenchyma. In fact, we successfully localized nodules up to 12 hours after injection of the contrast. This has practical implications given the unpredictability of surgical start times. When using this technique, one has to schedule the case to follow other earlier cases to allow for the radiotracer placement and postprocedure scintigram. We plan in the future to try radiotracer placement the afternoon before surgery to allow the thoracoscopic biopsy to be predictably scheduled as the first case of the day. Another advantage of the technique is the ability to reinsert the radioprobe through the stapler insertion site on the chest wall throughout the case to confirm that the lesion is in the resected specimen.

In conclusion, we have reported here our results using radiotracer localization and subsequent radioprobe-guided thoracoscopic excision in 46 patients with small, suspicious pulmonary nodules. Nodules were successfully localized and excised in 96% of the cases. Forty-six percent of these nodules were malignant, of which 71% were primary lung cancer. Although some benign nodules were excised, we believe that the yield of 33% primary lung cancers justifies the use of this technique in patients believed as a result of clinical and radiologic factors to be at risk for lung cancer.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
References
 
DR MALCOLM M. DECAMP (Boston, MA): I have one technical question. Can you comment on any of the radiation safety issues that you need to use with your operating staff? Secondly, you had 46% to 50% incidence of benign nodules in your series. One of your last conclusions was that the availability of this technique changes the "barometer" where you might want to intervene. Don't you think that 50% is too high a resection rate for lesions that turned out to be benign? I enjoyed the presentation very much.

DR STILES: Thanks. The radiation dose is fairly low. We don't do anything specifically to protect ourselves in the operating room. And the radiation cost, incidentally, added fairly little to the procedure. It's actually cheaper than an FNA (fine-needle aspiration) for these lesions. In terms of the second question, I'm sorry, can you repeat it?

DR DECAMP: It has to do with the high incidence of benign nodules resected.

DR STILES: I think that it's a little bit of a philosophy and you have to be willing, I think, to accept some benign lesions in order to find cancers earlier. I think certainly as we see more and more of these, we're getting better at picking out which ones are benign. A lot of things go into it, including things that don't necessarily make sense oncologically, things like patient anxiety or just our own suspicion that it's cancer. We would definitely like to decrease the amount of benign nodules that we resect, but at the same time we are showing that we can do it safely, with a low length of stay. We think that it's a good procedure.

DR RICHARD FEINS (Chapel Hills, NC): I enjoyed your presentation very much. This is a very neat technique. I guess my question comes up in terms of margins. It probably doesn't matter too much if you're going to go ahead and do a lobectomy, but for metastatic disease or for those patients who you might be doing who are not operable, it seems to me, as seemed to be the case on the nodule that you cut in your presentation, that when you're starting to go for these very deep, deep nodules that you might be compromising the margin compared to an open technique.

DR STILES: One way we get around that is by having the radiologists inject the radiotracer just deep to the lesion. This allows us a little bit of margin of error with respect to that. We haven't come across any tumors or nodules in our stapled margins yet. As you say for the cancers, other than for technical and oncologic purposes of not wanting to cut across a nodule, it doesn't particularly matter because all of those patients are going to go on to anatomic resection.

DR JOSEPH B. SHRAGER (Philadelphia, PA): One comment I have it that I would say that it likely does matter if you staple across a tumor and potentially spill it into the pleural space. That would certainly be one concern that I have as well.

But my actual question is, you mentioned that you usually felt first to see if you could feel the nodule, and then you went ahead and did the radioprobe analysis. What I would like to know is what percent of these couldn't you find with a finger that you then could find with the probe. In my view, the appropriate study to do actually would be let's feel it first and actually keep track of that and then see if this technique is allowing us to locate lesions not amenable to palpation.

DR STILES: We have started to do that. We didn't do it early on when we were just getting familiar with the technique. Doctor Daniel's guess is that we probably could have found about 40% of these with visualization and palpation alone.

DR CHUKWUMERE E. NWOGU (Buffalo, NY): In how many patients did the scintigram give you information that altered your management during the VATS (video-assisted thoracoscopic surgery) procedure? I wonder whether that is a cost-effective test.

DR STILES: Only in 2 patients in which the radiotracer was spilled. You can see diffuse signals in the pleural cavity in this picture in which we spilled the radiotracer. One way we have gotten past that problem is by having our radiologists inject a little deeper, particularly for the pleural-based lesions. And you may be right; it may be an extra test to do. It might not be necessary as we get better with it.

DR ARA VAPORCIYAN (Houston, TX): I have one question. Since all of these patients had a needle localization done transthoracically and over half of them were greater than a centimeter, what is the incidence of just getting a biopsy while the needle is in there and obviating the need for a thoracoscopy?

DR STILES: Well, I can tell you that our radiologists like doing this much better than they like doing FNA. I think that in skilled hands, particularly groups like the Cornell group, radiologists are able to reliably do FNA for these smaller lesions. It's not necessarily easy and it's fairly time-consuming, is my understanding. In contrast, this takes about 10 to 15 minutes. They don't have to worry about hitting the lesion. They just need to be close. They don't have to wait to send off the specimens. They would much rather do this quick and let us get the diagnosis than spend a whole lot of time doing FNA. We generally find that other groups say that their radiologists aren't particularly interested in FNA in these subcentimeter lesions either.

DR DAVID H. HARPOLE (Durham, NC): I have one question. I think this is great, and obviously you have a wonderful group of interventional thoracic radiologists who love doing procedures for you. Unfortunately that's not the case at a lot of institutions. How do you get them to schedule the CT (computed tomography) time, and do you do this like 2 or 3 days ahead and decide if it's going to be a first or second or third case and then set it up? How do you work out the logistics?

DR STILES: Well, we usually put it on at least second case because the radiologists get there later than we do, obviously. But they have been very cooperative and it has been very much a joint venture at UVA (the University of Virginia). The radiologists have actually put out a Web site where they have developed a sort of cookbook for this technique. We generally will get them to come in and do it as their first case. As we're getting better with it and as we're seeing some of these patients who are going out to longer times, we have discussed the idea of even doing it the day before. It remains to be seen if we'll be able to do that.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 

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