Computed Tomography-Guided Preoperative Radiotracer Localization of Nonpalpable Lung Nodules

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1 Computed Tomography-Guided Preoperative Radiotracer Localization of Nonpalpable Lung Nodules Massimo Bellomi, MD, Giulia Veronesi, MD, Giuseppe Trifirò, MD, Sarah Brambilla, MD, Luke Bonello, MD, Lorenzo Preda, MD, Monica Casiraghi, MD, Alessandro Borri, MD, Giovanni Paganelli, MD, and Lorenzo Spaggiari, MD Departments of Radiology, Thoracic Surgery, and Nuclear Medicine, European Institute of Oncology, Milan; and School of Medicine, University of Milan, Milan, Italy GENERAL THORACIC Background. We describe preoperative computed tomography (CT) guided injection of radiotracer technetium 99m macroaggregates ( 99m Tc-MAA) in challenging small lung nodules, intraoperative localization, and resection. Methods. Between November 2007 and February 2010, 44 patients with 47 lung nodules which were detected incidentally or at screening and that were 18 F-fluorodeoxyglucose positron emission tomography ( 18 F FDG- PET) positive or increasing in size at subsequent CT scans were candidates for surgical biopsy. Inclusion criteria for preoperative percutaneous CT-guided (lowdose technique) 99m Tc-MAA localization included having at least one of the following characteristics: nodule size less than 1 cm, subsolid morphology, or distance from the pleura greater than 1 cm. Results. Mean nodule size was 11 mm (range, 5 to 24 mm); 24 nodules were nonsolid, 15 nodules were partially solid, and 8 nodules had a solid morphology. Mean distance from the pleura was 11 mm (range, 0 to 35 mm). Localization complications included 13 minor asymptomatic pneumothoraces, 9 parenchymal hemorrhage suffusions, 1 mild allergic reaction to contrast medium, and 2 patients with chest pain after the procedure. Nine patients had mild extravasation of radiotracer into the pleura. In 2 cases, there was an extravasation of a significant quantity of radiotracer into the pleural cavity. Thoracoscopic biopsy was performed in 30 cases, 2 cases were converted to thoracotomy, and 12 patients underwent intentional thoracotomy. Conclusions. Asymptomatic subjects with suspicious nodules detected by screening or incidental CT are best candidates due to small lesion size and high percentage of nonsolid morphology, making thoracoscopic biopsy potentially difficult. Radiotracer localization is a safe, versatile, simple technique to help perform diagnosis with a minimally invasive approach in nonpalpable lung lesions. (Ann Thorac Surg 2010;90: ) 2010 by The Society of Thoracic Surgeons In the last decade, the increasing use of computed tomography (CT) in general clinical practice, improvements in CT technology, and the development of lung cancer screening programs have led to the detection of an increasing number of small lung nodules that were not previously identified with conventional radiology [1 3]. This has led to an increased number of surgical biopsies being performed, as CT criteria may not be sufficient to classify these lesions, which need a definitive histologic diagnosis [4]. Improvements in surgery have allowed surgical procedures to become less invasive. Video-assisted thoracoscopic surgery (VATS) is nowadays the procedure of choice to surgically biopsy and remove peripheral lung nodules. However, the use of VATS is limited by the difficulty in localizing small, deep, or nonsolid lung nodules where direct finger palpation may not be possible at surgery [5, 6]. Therefore, various techniques have Accepted for publication Aug 12, Address correspondence to Dr Bellomi, European Institute of Oncology, Via Ripamonti 435, Milan, 20141, Italy; massimo.bellomi@ieo.it. been developed to improve intraoperative localization of these nodules and achieve an adequate surgical resection while trying to keep morbidity as low as possible. Such techniques include percutaneous injection of liquid materials, including dyes such as methylene blue [7 9], India ink [10], lipiodol [11, 12], cyanoacrylate [13], colored collagen [14], barium sulphate and water-soluble contrast media [15, 16], percutaneous placement of hookwires [17 21], and fiber-coated or platinum microcoils [22, 23], image-guided navigational systems [24], ultrasoundguided surgery [25, 26], and preoperative bronchoscopically placed dyes [27]. These techniques, even with some limitations, have proven to be very useful in planning both investigation of and treatment for patients with small lung nodules. The technique of CT-guided percutaneous injection of radiotracer is not a novel technique; however, its use is limited to few centers. It was first described by Chella and colleagues in 2000 [28], and then further modified by Grogan and associates in 2008 [29]. Although our technique represents an evolution of a previously reported method, with some advantages, 2010 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur

2 GENERAL THORACIC 1760 BELLOMI ET AL Ann Thorac Surg RADIOTRACER LOCALIZATION OF LUNG NODULES 2010;90: there are only a few experiences reported in the literature. The aim of this study is to describe our technique of radiotracer localization of nonpalpable lesions and to report the results of our experience in terms of feasibility, safety, and efficacy of the procedure. Material and Methods Patient Selection Patients were enrolled both from a concurrent lung cancer screening program using low-dose CT (patients more than 50 years of age, current or former smokers) [30] and from the division of thoracic surgery of our institute. Our study was approved by our Institutional Ethical Committee, and written informed consent was obtained from all patients before enrollment in this study. The indication for surgical biopsy was the presence of an 18 F-fluorodeoxyglucose positron emission tomography ( 18 F FDG-PET) positive nodule or a nodule increasing in size at subsequent CT scans even if 18 F FDG-PET was negative. Patients were selected for percutaneous radiotracer injection if they had at least one of the following characteristics: nodule size less than 1 cm, subsolid morphology, or distance from the pleura more than 1 cm. Solid nodule morphology refers to nodules that completely obscure the entire lung parenchyma within them, as opposed to subsolid nodules that do not. A subsolid nodule can be further classified as either part solid (in the case of a nodule with patches of parenchyma that are completely obscured) or nonsolid (in the case of a nodule with no such areas) [31]. Patient selection was based on a clinical discussion in a multidisciplinary team meeting, involving thoracic surgeons, radiologists, and nuclear medicine physicians. We evaluated the feasibility of percutaneous CT-guided injection of radiotracer, the feasibility of a video thoracoscopic wedge resection versus an open wedge resection according to distance of the lesion from the pleura and hilar structures, and the possibility to improve localization of the nodule with an intraoperative gamma probe. the needle entry point were distance between skin and lung nodule, bone and muscle structures interposed between entry point and lung nodule, and presence of lung fissures interposed between entry point and lung nodule, to avoid crossing two different lobes during needle insertion. After injection of local anesthetic, the correct placement of the tip of a 25G needle in or near the nodule was eventually verified with a further series of 12 to 20 images. Once this was confirmed, 0.2 to 0.3 ml of a solution composed of 0.1 to 0.15 ml 99m Tc-MAA and 0.1 to 0.15 ml nonionic iodinated contrast medium was injected. A further CT scan was performed to define the distribution of the contrast medium, which also allowed us to check for any iatrogenic pneumothorax (Figs 1 and 2). The patient was then transferred to the nuclear medicine department to confirm the correct placement of the 99m Tc-MAA by performing a scintigraphy (Fig 3). Lateral and anterior scintigraphic images were acquired. A flexible wire 57 Co source was used to outline the body region contour during acquisition. Both images were obtained with the patient supine. Images were acquired over approximately 5 minutes, collecting 70 kcounts in a pixel matrix, zoom 1.33, to check possible migration or contamination areas. When the hot spot appeared as a small, well-delimited area, the patient was referred for surgery. Surgical Procedure The surgical procedure was performed within 24 hours from the nodule localization with 99m Tc-MAA, either on the same day or the next day. The patient was placed in the lateral decubitus position, and single lung ventilation Preoperative Localization Technique The radiotracer chosen for the localization procedure was 99m Tc-MAA (MAASOL; GE Healthcare, Buckinghamshire, UK) with a half life of 6.02 hours and particle size of 10 m to 100 m. Depending on the time interval between localization and the planned surgery, 4 g to9 g human serum albumin macroaggregates labelled with 7 to 15 MBq freshly eluted 99m Tc-MAA, together with 0.1 to 0.15 ml nonionic iodinated contrast medium, were injected under CT guidance. Radiolabelling and quality control were performed according to the manufacturer s instructions. To establish the best approach to correctly localize the nodule, the patients underwent a CT scan without contrast medium (220 to 270 ma, 120 kv, slice thickness 2.5 mm, pitch 1.35). The factors considered when choosing Fig 1. Axial computed tomography scan of a 55-year-old patient showing a 9-mm nonsolid lung nodule in the superior lobe of the right lung.

3 Ann Thorac Surg BELLOMI ET AL 2010;90: RADIOTRACER LOCALIZATION OF LUNG NODULES Fig 2. Axial computed tomography scan of the same patient after injection of contrast medium and radiotracer, showing iodinated contrast medium in the area of the nodule. performed. After introduction of a videothoracoscopic camera, usually in the VII intercostal space, and either an anterior utility thoracotomy of 3 cm (VATS technique) or a lateral muscle-sparing thoracotomy (open technique), the exact location of the nodule was identified by passing an endoscopic gamma detecting probe (Neo 2000; Neoprobe, Dublin, OH) over the surface of the involved lung. The identification of the nodule was based on the maximum signal intensity by both a numeric and an acoustic signal. After its identification, resection of the nodule using automated stapling devices (EndoGIA Universal; Covidien, Norwalk, CT) was performed. The removed nodule was examined at frozen section. According to the pathologic nature of the nodule after histologic examination, the appropriate surgical procedure was performed. Results 1761 Between November 2007 and February 2010, 44 patients with 47 lung nodules underwent CT-guided radiotracer placement for nonpalpable lung nodules followed by radio-guided surgical biopsy. There were 22 male and 22 female patients with a mean age of 61 8 years (range, 38 to 75). Overall, 47 lung nodules were localized; in 3 patients, localization of 2 lung nodules was done during the same sitting. The mean size of the nodules, as measured on CT, was 11 5 mm (range, 5 to 24 mm). The mean distance from the outer edge of the nodule to the nearest pleural surface was 11 9 mm (range, 0 to 35 mm). The anatomical location and morphology of these nodules can be seen in Table 1. The average time taken for the localization procedure was 19 minutes (range, 11 to 42). In 24 localization procedures, no complications were reported. Complications recorded included 13 minor asymptomatic pneumothorax, which did not require any intervention other than observation; 9 cases of parenchymal hemorrhage suffusion, which did not need any surgical intervention; 2 cases of chest pain after the procedure, and 1 mild allergic reaction to the percutaneous injection of contrast medium. The localization scintigraphy performed immediately after the procedure showed that 9 patients had a mild extravasation of radiotracer into the pleura; however, that did not interfere with the detection of radiotracer at surgery. In 2 other cases, there was an extravasation of a significant quantity of radiotracer in the pleural cavity that would have not allowed an accurate identification of the marked nodule during surgery, and therefore, it was decided to repeat the procedure at a later date. The repeat procedure successfully localized the nodule in both patients, 1 of whom had a small asymptomatic pneumothorax. Fourteen patients underwent surgery on the same day of the localization procedure, and 30 patients underwent surgery the day after the localization procedure. Thirty patients had a videothoracoscopic surgical biopsy performed. In a further 2 patients, the videothora- GENERAL THORACIC Fig 3. Thoracic scintigraphy: (A) anterior view and (B) right lateral view of the thorax showing a hot spot (site of injection) and body contour from a flexible wire 57 Co source.

4 GENERAL THORACIC 1762 BELLOMI ET AL Ann Thorac Surg RADIOTRACER LOCALIZATION OF LUNG NODULES 2010;90: Table 1. Nodule Morphology and Location Nodule Morphology Number Nodule Location Number Solid 8 Right upper lobe 16 Partially solid 15 Right middle lobe 3 Nonsolid 24 Right lower lobe 8 Left upper lobe 14 Left lower lobe 6 Total 47 nodules Total 47 nodules coscopic procedure was converted to a minithoracotomy and a thoracotomy to identify the localized lung nodule. For 12 patients, the surgical biopsy was performed under intentional thoracotomy. The surgical procedure was then completed according to the result of the frozen section examination. Of the 30 patients who had videothoracoscopic surgical biopsy performed, 13 had the final surgical procedure after frozen section completed with the Da Vinci Robot (Intuitive Surgical, Sunnyvale, CA), and 8 of them were converted to thoracotomy. The histologic nature of the nodules biopsied can be seen in Table 2. Comment Clinicians are faced with an increasing number of suspicious lung nodules that need to be characterized by biopsy. Nowadays, VATS plays a central role in the surgical biopsy of suspicious lung nodules [32]. However, the lack of digital palpation in small, subsolid, and deep nodules may cause inability to accurately identify small lung nodules. When lung nodules are not identified intraoperatively at VATS, the procedure has to be converted to an open thoracotomy; thus, there is an indication to preoperatively localize small nodules that are distant from the pleural surface [5, 6]. In a study involving 92 patients, Suzuki and coworkers [5] showed that if the distance to the pleural surface was greater than 5 mm for lesions measuring 10 mm or less in size, the probability of failure to locate the nodule and having to convert to thoracotomy was greater than 50%. One of the first described localization techniques suggested the use of hookwires for breast nodules [33]. For pulmonary nodules, percutaneous placement of hookwires [17 21] and fiber-coated or platinum microcoils [22, 23] have been used. Potential complications have included bleeding with hematoma formation, pneumothorax, heamothorax, and dislodgement of the hookwire, which may occur before surgery or during placement of the patient in the operating theater [17, 20, 22]. Rare cases of significant air embolisms have also been described [34]. Using stiff hooks could also potentially interfere with frozen section examination if this alters the specimen. If hookwires cross any lung fissures, they may complicate thoracoscopic resection as it forces the surgeon to approach the nodule through the hook path, when the optimal surgical approach could be through a different site. Another localization technique involves the percutaneous injection of various types of liquids. A general complication is that they can diffuse in the lung and pleural cavity in the time interval between localization and surgery, thus making localization at surgery difficult. These liquids include dyes such as methylene blue, which is injected on the pleural surface of the underlying nodule. This technique does have some limitations, including the possibility of anaphylactic reactions and difficulty in visualization of the dye at surgery in the presence of extensive anthracotic pigmentation, and it does not provide any information on the depth of the nodule from the pleural surface [7 9]. Other liquids such as India ink, iodine, barium, lipiodol, and cyanoacrylate have been previously used [10, 12 16]. When injecting liquids that are not water soluble, there is a potential risk of embolism and cerebrovascular accidents if these inadvertently reach the systemic circulation [12]. The use of bronchoscopically placed dye under CT guidance to localize nodules requires skills and expertise that are not readily available in many centers [27]. The use of radioopaque liquids to localize nodules also requires the use of intraoperative fluoroscopy in the operating theater to identify the nodule, exposing the surgical team and the patient to further radiation. Intraoperative localization of nodules can be performed under ultrasonographic guidance. To visualize nodules sonographically, the lung must be collapsed. Localization of small nodules in patients with emphysematous lungs is not reliable as it may be difficult to completely collapse the lung. It is a time-consuming procedure and requires experienced and skilled operators owing to the potential presence of artifacts [26, 35 37]. Few experiences are reported in literature using the percutaneous injection of radiotracer [29, 38 40]. In our institute, we have utilized this technique since 1996 [41] to localize nonpalpable breast lesions. We modified the technique described by Grogan and coworkers [29] by adding a small amount of nonionic iodinated contrast medium to the radiotracer. This method, through a further low-dose CT scan performed at the end of the procedure, allows visualization of contrast medium distribution in relation to the nodule and therefore better guides the intraoperative localization performed by the surgeon, who can orient the resection according to the Table 2. Histologic Outcome of Nodules Biopsied Histology Number Adenocarcinoma 36 Squamous cell carcinoma 1 Small cell carcinoma 1 Lymphoma 1 Carcinoid 1 Hamartoma 1 Atypical adenomatous hyperplasia 2 Anthracotic lymph node 1 Fibrotic-inflammatory 3

5 Ann Thorac Surg BELLOMI ET AL 2010;90: RADIOTRACER LOCALIZATION OF LUNG NODULES relative position of the nodule and the contrast. This method also highlights the importance of adequate communication between the multidisciplinary team members to adequately plan both the localization procedure and the surgery. In our experience, the rate of detection through videothoracoscopic approach was high (only 2 cases of conversion). Even during the open approach, the methods were useful for the correct localization of the nodule, which was resected through simple wedge resection or typical segmentectomy. The complication rate of the procedure was low, and the technique was simple and effective. Our use of the localization procedure for both VATS and thoracotomy shows that this is a versatile technique that can be applied to various surgical approaches. From the results of our experience, we can confirm that percutaneous injection of radiotracer has some advantages compared with other techniques. The radiotracer used, 99m Tc-MAA, is readily available as it is the same tracer used for pulmonary perfusion scintigraphy and its properties are already well known. In addition, it does not interfere with frozen section or histologic examination. The half life of this radiotracer makes it ideal for use in the subsequent thoracoscopic excisional biopsy as it allows enough time for the procedure to take place, and the marker can still be detected at VATS. By adding 0.1 to 0.15 ml iodinated contrast medium to the radiotracer, it is possible to obtain a precise map of the anatomical landmarks and the nodule by CT, in addition to scintigraphy. Regarding the technique, there is no insertion of foreign bodies within the lung, and therefore no risk of dislodgement or transfissural positioning. This frees the surgeon to use the best surgical approach, as the lesion can be approached from the point that provides the shortest distance between nodule and pleura. The use of gamma probes to detect the nodules during surgery is a simple time-saving procedure. After surgical removal of the lung nodule, it is also possible to confirm that the marked nodule is in the resected specimen by passing the gamma probe over the specimen and identifying it as a hot spot. The whole protocol of localization and surgery utilizes resources and expertise that are already available in many centers: CT, radionuclide, scintigraphy, gamma probes, and VATS. There is also a greater flexibility in coordinating the localization procedure with surgery because it can be performed the morning after the injection of the radiotracer. There are limitations to our study. There is an inherent risk of pneumothorax when performing the percutaneous injection of radiotracer. Also, because we use iodinated contrast medium, even though in very small quantities, there is still a risk of allergic reactions. Another limitation is that we do not have values for the number of counts detected on the gamma probe during the surgical localization of the nodule; however, the surgeon was always able to detect the nodule in the operating theater using the probe. In conclusion, the technique proposed is a useful versatile tool in the diagnostic workup and treatment of patients presenting with small lung nodules that offers new alternatives to thoracic surgeons in the clinical approach to these patients. It utilizes readily available resources, integrating the skills of several specialties to further improve treatment protocols already available. References Market summary report. DesPlains, IL: IMV Medical Information Division; Yankelevitz DF, Henschke CI. Small solitary pulmonary nodules. Radiol Clin North Am 2000;38: Remy-Jardin M, Remy J, Giraud F, Marquette CH. 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Ann Oncol 2002:13; INVITED COMMENTARY The current study by Bellomi and colleagues [1] describes the feasibility and outcomes of the percutaneous injection of radiotracer (technetium-99 macroaggregated albumin) for localization of indeterminate pulmonary nodules. The authors successfully implemented this technique to resect 47 lesions (mean size, 11 5 mm) in 44 patients. Of these, 30 patients underwent video assisted thoracoscopic pulmonary resection, whereas 12 patients experienced an intentional thoracotomy. The need for localization during intentional thoracotomy is not clearly explained; however, pure ground glass opacities are difficult to palpate regardless of the surgical approach. Neoplastic disease was detected in 85% (40 of 47) of the pulmonary nodules, emphasizing the importance of patient selection for this localization technique. Although this study is similar to the few previously published reports [2, 3], the authors confirm the results of a modality that is seldom implemented for the detection of small, deep nodules that are difficult to palpate by a thoracoscopic technique. Complications were minor, highlighted by small pneumothorax (28%), limited parenchymal hemorrhage (19%), and radiotracer extravasation (4%). Two patients underwent repeat localization due to inadvertent radiotracer placement. No deaths were reported in this series. Despite the availability of technetium radiotracer and gamma probes in many institutions by virtue of sentinel node detection in the management of breast cancer, this diagnostic technique has limitations that are not fully appreciated in the published series. Small central lesions cannot be routinely accessed by percutaneous computed tomography guidance. Lesions exceeding 1 cm positioned in the periphery of the lung can often be considered for diagnostic computed tomography-guided fine needle aspiration, thus establishing the need for anatomic resection preoperatively. Interestingly, this series and others describe the use of this localization technique in lesions ranging from 3 to 24 mm. One could argue that lesions that reach 20 mm should be palpable (particularly with mixed solid and ground glass characteristics), thus precluding the use of any localization modality. In summary, detection of subcentimeter nodules is a more frequent event given the wide availability of highresolution computed tomography. Radiotracer localization of indeterminate pulmonary nodules can be useful if the nodules are deemed nonpalpable. Alternative localization 2010 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur