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1 Department of Radiology, Brigham and Women's Hospital, Boston, MA 02115.
2 Department of Radiology, Dana Farber Cancer Institute, Harvard Medical School,
44 Binney St., Boston, MA 02115.
3 Present address: Department of Radiology, University of Massachusetts Medical
Center, Worcester, MA.
4 Department of Surgery, Brigham and Women's Hospital, Boston, MA 02115.
5 Department of Surgery, Dana Farber Cancer Institute, Harvard Medical School,
Boston, MA 02115.
6 Present address: University of Washington Medical Center, Seattle, WA.
7 Department of Medical Oncology, Dana Farber Cancer Institute, Harvard Medical
School, Boston, MA 02115.
Received April 16, 2004;
accepted after revision August 10, 2004.
Address correspondence to E. vanSonnenberg
(ericvansonnenberg{at}yahoo.com).
Abstract
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MATERIALS AND METHODS. Our cohort consisted of 30 patients with a spectrum of primary (n = 18) and secondary (n = 11) lung tumors, mesothelioma (n = 1), and five secondarily eroded, painful ribs who underwent ablation of 36 total lesions (one patient had two ablations). Patients either were nonsurgical candidates because of medical comorbidities or extent of disease, or had exhausted chemotherapy and radiation therapy options, or had refused surgery or undergone unsuccessful surgery. Patients were treated with radiofrequency ablation after agreement among oncologists, thoracic surgeons, and interventional radiologists. An array-style electrode under impedance control was used to treat 29 thoracic tumors and the adjacent rib metastases (n = 5). A cool-tip radiofrequency probe was used for two patients. CT guidance and general anesthetic were used for all but one patient. Sonographic guidance and IV conscious sedation were used in one patient. Pain (n = 11) and tumor cure or control (n = 19) were the primary indications for the procedures. Adjunctive procedures to the radiofrequency ablations included the creation of saline or water windows (n = 3); establishment of transosseous and transchondral routes (n = 4); use of intercostal and paravertebral nerve blocks (n = 15); and use of an intraprocedural catheter (n = 1), needle (n = 1), or sheath (n = 3) for treatment of pneumothoraces. Follow-up was from 2 to 26 months.
RESULTS. All ablations were technically successful. No periprocedural mortality occurred. Necrosis of tumor was greater than 90% in 26 of 30 lesions based on short-term follow-up imaging (CT, PET, MRI). In the 11 patients who underwent ablation for pain, relief was complete in four and partial in the other seven. One patient developed a local skin burn, four patients had self-limited hemoptysis up to 4 days after ablation, one had transient atrial fibrillation, one developed hoarseness, and two patients were transiently reintubated after extubation. Eight pneumothoraces developed; one patient underwent placement of a chest tube. Four patients died within 1 year of ablation from extrathoracic spread of tumor.
CONCLUSION. Radiofrequency ablation for a variety of thoracic tumors can be performed safely and with a high degree of efficacy for pain control and tumor killing. The effect of ablation can be assessed with CT, MRI, or PET. Various technical issues differentiate thoracic tumor ablation from standard abdominal ablations. Numerous other thoracic interventional radiology procedures are beneficial to assist the radiofrequency ablation. A multidisciplinary approach offers valuable expertise for patient care.
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This article describes our experience in the initial 30 patients who underwent ablation of 36 thoracic lesions. Relevant clinical and technical aspects, results, and complications are detailed. Associated issues and problems prompted use of numerous adjunctive thoracic interventional radiology procedures. Multidisciplinary input from various services is emphasized in overall patient care.
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Each patient was evaluated by a faculty member from the departments of surgery (thoracic division), medical oncology (thoracic division), anesthesiology, and radiology (tumor ablation group of interventional radiology). Ablation was done only when the evaluating team reached unanimity.
Of the 30 patients, 17 were men and 13 were women. The patients' ages ranged from 29 to 89 years (mean, 64.5 years). Eighteen patients had bronchogenic carcinoma, 11 had metastatic disease, and one had mesothelioma of the pleura. The types of lung cancer were non–small cell (n = 13) and squamous cell (n = 5) carcinoma. The primary lesions in patients with metastatic disease were as follows: one patient each with adenoid cystic carcinoma of the parotid gland, the tongue, and the lacrimal gland; squamous cell carcinoma of the tongue; hepatocellular carcinoma; renal cell carcinoma; prostate carcinoma; cystosarcoma phylloides of the uterus; pleomorphic sarcoma; and adenocarcinoma of the colon (two cases). The sites of the tumors in the 29 patients with lung lesions were 14 right lung, 15 left lung; 14 upper and 12 lower lobe, three right middle lobe and lingula; and 18 peripheral versus 11 central (within 2 cm of the hilum) lesions. One 39-year-old man had a chest wall lesion from an incurable thoracic mesothelioma. Clinical data are summarized in Table 1.
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Twenty patients had underlying emphysema from their smoking history. Primary indications for the procedures were for tumor cure or palliation (n = 19) and to treat pain (n = 11). Pain was quantified subjectively before and after ablation on a scale of 1–10. Five patients had simultaneous treatment of adjacent metastatic rib lesions from local invasion by their lung tumors (Fig. 1A, 1B, 1C). Fifteen patients had undergone surgery previously, 21 patients had chemotherapy, and 13 patients had radiation therapy before the radiofrequency ablation. Two patients had undergone attempted resections of their lesions that were unsuccessful and led to referral for ablation.
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The ablation procedures were performed with CT fluoroscopic guidance (Siemens Somatom Plus 4) in 29 patients; sonography was used in one patient. Angling of the CT gantry was used to optimize access to the tumors in 13 patients. Multi-planar CT reconstruction was used in three cases to highlight and verify probe position with respect to adjacent anatomic structures (Fig. 2A, 2B).
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The radiofrequency procedures were performed with an array-type electrode (LeVeen electrode, Boston Scientific) with diameters of 2–5 cm, except two patients whose procedures were performed with a cooled-tip needle probe (Cool-Tip, Radionics). A coaxial introducer was used in four patients with the LeVeen system.
Power from the radiofrequency generator (RF 3000, Boston Scientific) was delivered in a stepwise algorithm that provided starting powers of 20–80 W and increased 5–10 W/min to maximum values of 55–200 W. End points for ablation were dramatic increase in impedance (termed "roll-off" by the manufacturer) with the Boston Scientific device, and an elapsed time of 12 min (per the manufacturer's instructions for use) with the Radionics device.
In 29 patients, anesthesia was general, with endotracheal intubation. Double-lumen endotracheal tubes were used in three patients by personal preference of the attending anesthesiologist. IV conscious sedation was used in the first patient. All patients received one dose of antibiotics for the procedure and two doses afterward: 28 patients, IV cefazolin (1 g); one patient, IV levofloxacin (500 mg); and one patient, vancomycin (1 g).
Laboratory workup included a complete blood count, serum chemistries, and coagulation studies (electrolytes and prothrombin time, partial thromboplastin time, platelet count, and international normalized ratio). Coagulation results were normal before the procedure in all patients. Twenty-eight patients underwent diagnostic biopsy with 25- or 22-gauge needles in the same session just before the radiofrequency ablation procedure [17, 18]. Corroborative tests were highly suggestive of malignancy; hence, to save an extra procedure, the biopsy was performed just before the ablation.
In all patients, the imaging workup included contrast-enhanced CT and chest radiography within 2 months before the procedure. One patient who had a creatinine level of 2.7 mg/dL had 60 mL of gadopentetate dimeglumine used for IV contrast material at CT instead of iodinated material. Twenty-four of 30 patients underwent PET before radiofrequency ablation, and 10 patients after the ablation. Fourteen patients underwent gadolinium-enhanced MRI before, and 12 patients after, the ablations. Percentage of necrosis of the tumor on postprocedure scans was determined by consensus of three radiologists. Contrast-enhanced CT was performed immediately after the radiofrequency ablation in all patients in whom CT was used for guidance. All patients had follow-up with chest radiography, the initial one done in the recovery room after the procedure.
Forty-eight ancillary procedures or maneuvers were performed to improve lesion access, relieve pain, or decrease the risk of complications (Table 2). The saline window technique [19] was performed in three patients with severe emphysema to displace overlying lung, thereby allowing a direct extrapulmonary approach into the lesions. Distilled water was used as a modification in the latter two of the three patients to reduce the conductive effect of radiofrequency. The "salinoma" was created anteriorly, and the two "hydromas" were created posteriorly (Fig. 3A, 3B, 3C).
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In four patients, a transosseous route (through abnormal [n = 3] or normal ribs [n = 1]) was used, whereas a transcartilaginous approach was opted for in a fourth patient for access. In the transosseous route through a normal rib, a 14-gauge Bonopty needle (Radi Medical Systems) was used to drill a hole through the rib through which the radiofrequency ablation probe was inserted (Fig. 4A, 4B, 4C).
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The five patients who underwent associated rib ablations received a total of nine intercostal and paravertebral nerve blocks with 3–5 mL of bupivacaine HCl 0.25% (AstraZeneca) immediately after the radiofrequency ablation. Two patients with painful subpleural tumors underwent a total of six intercostal nerve blocks after the ablation, and two blocks were performed in a patient with chest wall invasion.
One patient with a carcinoma against the mediastinum and juxtaposed to the trachea had cool distilled water placed and exchanged into the cuff of the endotracheal tube during the ablation to help protect the trachea by providing an added heat sink. One patient underwent evaluation of a cardiac defibrillator by cardiology consultants because of concern about possible interference from the radiofrequency ablation procedure. Deactivation of the defibrillator for the procedure was achieved by placing a magnet over it before the ablation. Another patient had a lesion near the heart that required careful probe placement to avoid potential arrhythmias [15] (Fig. 5).
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The approach to the lesions did not traverse lung parenchyma in 17 patients and did in 13 patients. The salinoma or hydroma technique effectively provided an extrapleural route in the three patients in whom it was used; none of these patients developed a pneumothorax. One of these procedures was performed anteriorly (50 mL of saline), and the other two posteriorly (40 and 100 mL of distilled water, respectively).
Maximum impedance with roll-off was achieved in 24 patients, between 5 and
75 min. Second radiofrequency applications were done in 18 patients in whom
roll-off was achieved. In 21 of 30 patients, repositioning of the
radiofrequency probe and more than one burn were performed in the same
session. The maximum number of sites of radiofrequency treatment was five in
one patient. Mean impedance just before roll-off was 65 
..
Patients were hospitalized on the thoracic surgical service from 1 to 12 days (mean, 1.8 days); 26 of 30 patients left the hospital 1 or 2 days after the procedure. Patients were followed up for 2–26 months. There was no 30-day mortality. Four patients died of extrathoracic spread of disease at 3, 4, 6, and 9.5 months.
A total of 15 complications occurred (Fig. 7A, 7B, 7C, 7D). These included eight intraprocedural pneumothoraces; no patient had oxygen desaturation. A 5-French sheath (Yueh System, Cook) restored the position of the tumors in three patients to allow the procedures to continue; the sheaths were removed at the end of the ablation. A 7-French chest catheter (Boston Scientific) was inserted to restore the position of the lesion that had moved and to continue the radiofrequency ablation procedure in one patient; the catheter was removed 1 day after the procedure. Needle aspiration (18 gauge) was used to evacuate the pneumothorax (25%) in another patient after the radiofrequency procedure was completed. No therapy was required for three other patients who had less than 10% pneumothoraces. All pneumothoraces developed in transparenchymal approaches to the tumors.
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One elderly patient with a peripheral tumor developed atrial fibrillation after the procedure, which was controlled medically. Two elderly patients with severe emphysema were reintubated after extubation because of respiratory difficulty after the radiofrequency ablation; both recovered after 5 and 12 days, respectively, of hospitalization. One of these patients eventually underwent a tracheostomy.
Two to four days after the ablation, four patients developed mild hemoptysis. One patient underwent bronchoscopy by the surgical team, but no lesion was found. No further bleeding occurred in these patients. No patient required a blood transfusion. None of these lesions was central.
One patient developed a 1-cm third-degree skin burn. This complication was thought to be due to conduction along a 22-gauge needle that was left in the patient during the ablation early in our experience. The patient underwent local surgical débridement and then healed normally.
One patient became hoarse the day after treatment of a bronchogenic carcinoma near the aortic arch. Vocal cord paralysis was seen by direct laryngoscopic vision. Gelfoam (gelatin sponge, Upjohn) injection into the vocal cord improved speech [20] the same day, although mild hoarseness persisted for 2 months. The closest tumor to the heart that was ablated was 8 mm away; this patient suffered no ill effects from the successful ablation.
Imaging follow-up was helpful to indicate the need for further ablation (n = 1) or for nonaction when the tumors were treated adequately (n = 29) (Fig. 8A, 8B, 8C, 8D, 8E, 8F, 8G, 8H). Postprocedure PET showed loss of virtually all FDG activity in the previously positive areas in nine of 10 patients. In one patient, a repeat ablation was performed on the basis of persistent FDG avidity on PET and subsequent positive biopsy. MRI revealed reduced or no enhancement on dynamic imaging compared with the preprocedure MRI, indicative of necrosis in all 12 patients in whom the study was performed after ablation. Follow-up contrast-enhanced CT after 3 months in 19 patients showed persistent necrosis (13 patients), tumor shrinkage (seven patients), cavitation (six patients), and tumor recurrence (one patient). Shrinkage was up to 1 cm in six patients, and one patient had a 2-cm decrease in diameter of the original tumor. Cavitation was seen on both CT and chest radiography follow-up.
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Long-term patient survival after radiofrequency ablation for thoracic tumors was not determined in our study because the longest follow-up was only 26 months. Therapeutic efficiency was manifested by amelioration of pain in all patients after the radiofrequency ablation, both in the thoracic lesions and the locally invaded rib metastases. Extensive necrosis of tumor was achieved in all patients on follow-up CT and MRI examinations. Almost all patients who underwent PET before and after ablation had complete loss of FDG activity after ablation. Positive postablation PET findings were used to indicate the need for a second ablation because of persistent tumor in one patient. A recent study suggests CT densitometry may be valuable to assess the effects of radiofrequency ablation in the thorax [21].
The literature on percutaneous ablation of thoracic tumors is still early and developing. Several surgical [11, 12] and radiologic [10, 13–16, 22] laboratory studies showed encouraging results with radiofrequency [10–12, 15, 16] and laser [22] heating in either normal parenchyma [10, 12, 16, 21] or experimental tumors [11, 13–15] in the lungs. The clinical reports on ablation of lung tumors began with a study of three patients by Dupuy et al. [1] in 2000. Early small series and case reports of patients have focused on feasibility and complications [1–9]. A report of 20 patients with colorectal pulmonary metastases described a 50% pneumothorax rate, and 25% of these patients required a chest tube [23].
Complexities of thoracic intervention, such as approach to the lesions, management of potential and actual complications, and treatment of related lesions, provided the opportunity to use adjunctive interventional radiology procedures to supplement and facilitate the ablations. Access to the lesions was aided by four techniques: catheter, sheath, or needle evacuation of pneumothorax to restore lesion position; CT gantry angulation; salinoma (or hydroma) window creation to allow an extrapulmonary approach to lesions in patients with severe emphysema who were at risk for pneumothorax that might require chest tube drainage; and transosseous and transcartilaginous approaches when lesions were shielded by overlying bone. The need to restore the pulmonary tumor to its original position for radiofrequency ablation after a single needle puncture (with a 22-gauge needle) that produced a pneumothorax necessitated a 7-French chest tube in one patient, an 18-gauge needle in a second patient, and a 5-French sheath in three patients from 25-gauge needles. The salinoma or hydroma technique permitted avoidance of emphysematous lungs by the 15-gauge radiofrequency ablation probes in three patients, likely avoiding pneumothoraces. As with percutaneous biopsy of lung tumors, whenever possible, access that avoided normal lung always was chosen, and is recommended.
The ablation procedure provided relief (partial, n = 7; complete, n = 4) in all 11 patients who had pain from their lesions. Five patients who had painful rib lesions from direct tumor erosion caused by the adjacent peripheral lung tumors underwent ablation of the osseous lesions in the same setting. In these latter patients, intercostal and paravertebral nerve blocks with long-acting local anesthetic were used to help prevent postprocedure discomfort; similarly, intercostal nerve blocks were used in two patients with chest wall invasion and a subpleural tumor, respectively. None of these patients had any significant postprocedure pain.
Several other specific issues were dealt with by anesthesiologists and cardiologists. Although most anesthesiologists used a single-lumen endotracheal tube, some preferred a double-lumen tube to isolate each individual lung. However, no clinical problem mandated selective use of the double-lumen endotracheal tube. An alternative to the use of general anesthetic with endotracheal tube intubation is IV conscious sedation, which we used in one patient. General anesthesia offers the benefits of no intraprocedural pain, no movement by the patient, and full respiratory control by the anesthesiologist; thus, general anesthesia was our choice routinely. Nonetheless, we had two elderly patients who needed reintubation because of respiratory distress after the procedure and general anesthesia; both had severe emphysema and each recovered after 5- and 12-day hospitalizations.
In one patient whose tumor was against the trachea, cool distilled water was placed and exchanged in the endotracheal tube cuff during the ablation to help protect the trachea from the heating effect.
Proximity of a cardiac defibrillator with possible interference by the radiofrequency system did not contraindicate the procedure in one patient [24]. Disabling of the device during the procedure and reprogramming afterward were performed by the consulting cardiology team.
The safety and feasibility of clinical radiofrequency ablation of thoracic tumors are further documented by this study. Pain associated with these tumors can be palliated. Substantial necrosis of the tumors was documented by imaging studies. Various and diverse adjunctive procedures for thoracic ablations are technically beneficial and expand the options for treatment. Ongoing series are anticipated to further ascertain the overall role of radiofrequency ablation in the management of thoracic malignancy. Coordinated multidisciplinary teamwork provides valuable expertise in patient selection and clinical care for these patients. Thus, radiofrequency ablation has increased therapeutic options for patients with thoracic malignancies.
Acknowledgments
We thank Sue Ellen Lynch and Janice Galinsky for their assistance.
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