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Original Report |
1 Department of Diagnostic Imaging, Rhode Island Hospital, Brown Medical School,
593 Eddy St., Providence, RI 02903
2 Department of Radiation Oncology, Rhode Island Hospital, Brown Medical School,
Providence, RI 02903.
Received February 14, 2003;
accepted after revision March 25, 2003.
Address correspondence to D. E. Dupuy
(ddupuy{at}lifespan.org).
Abstract
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CONCLUSION. Percutaneous radiofrequency ablation in conjunction with brachytherapy is a promising minimally invasive combination modality. It may be a treatment option for patients with primary, recurrent, or metastatic malignancies of the lung that are not amenable to surgery or further external beam radiation therapy.
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Brachytherapy—alone or in combination with external beam radiation therapy or chemotherapy—to supplement radiation doses (boost technique) is particularly well suited for use in patients with either metastatic lung malignancies or prior treatment that precludes additional external beam radiation therapy [3-5]. Radioactive sources, referred to as "seeds," are either temporarily or permanently implanted into the tissue directly (interstitially) or into a body cavity (intracavitary). Brachytherapy can be used for local cure or palliation or in the adjuvant setting with surgery or chemotherapy in the treatment of lung cancer [3, 4]. Dose rates are classified as either low or high. Low- and high-activity iridium-192 (192Ir) or high-activity iodine-125 (125I) seeds are used in temporary implants, and low-activity 125I seeds are used in permanent implants [5].
Percutaneous imaging-guided tumor ablation with radiofrequency is an expanding minimally invasive modality for the local treatment of solid malignancies. First reported in humans in 2000 [6], radiofrequency ablation of lung tumors may be a promising treatment option for nonsurgical candidates given the suboptimal outcomes with current treatment options. The insertion of a radiofrequency electrode into the defined tumor bed and the establishment of an electric field to a reference electrode that oscillates with generated alternating radiofrequency currents ultimately create a conduit for frictional heating [7]. Tissue heating consequently induces coagulative necrosis and cell death, including destruction of centrally located hypoxic tumor that is typically less responsive to chemotherapy and radiation therapy [7, 8]. The surrounding air in the normal parenchyma of the lung acts as an insulator and concentrates radiofrequency energy in the targeted tissue, requiring less energy deposition [9]. Although radiofrequency ablation alone is a possible treatment, concern remains about the presence of viable tumor persisting at the periphery because aerated lung diminishes the conduction of radiofrequency current and heat. To counteract this principle, we combined radiotherapy in the form of brachytherapy to provide more definitive local therapy.
The tumoricidal effects of hyperthermia have been discussed in radiofrequency ablation [7] and implemented via microwaves in combination with brachytherapy [8]. Our institution recently reported experiences with brachytherapy performed at the time of radiofrequency ablation [10]. To our knowledge, this combination in the treatment of solid malignancies has not been reported previously. In this report, we present the clinical experience of three patients undergoing this procedure, with available follow-up ranging from 1 to 12 months.
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The first patient was a 78-year-old man diagnosed in 2001 with T4 N1 M0 poorly differentiated squamous cell carcinoma of the lung. Initial chest CT revealed a 4-cm mass in the left upper lobe abutting the mediastinum and left hilar lymphadenopathy (Figs. 1A, 1B, 1C, 1D, 1E, and 1F). Bronchoscopy showed diffuse erythema, and brushings yielded cells consistent with non-small cell lung cancer. The patient was not considered a candidate for surgery initially because of probable invasion of the primary tumor into the mediastinum. Induction treatment with paclitaxel (Taxol, Bristol-Myers Squibb, Princeton, NJ) and carboplatin (Paraplatin, Bristol-Myers Squibb) and external beam radiation therapy for 6 weeks (total dose, 50.40 Gy) were undertaken. At the completion of chemotherapy and external beam radiation therapy, the patient was not considered to be a surgical candidate because of respiratory compromise. Although the patient had a dramatic response to the initial therapy, local progression was detected at 14 months. Biopsy confirmed recurrent non-small cell carcinoma. Positron emission tomography showed increased activity in the region of the patient's known lung tumor in the left upper lobe. The 3.0-cm mass was treated with radiofrequency ablation and high-dose-rate brachytherapy (Figs. 1A, 1B, 1C, 1D, 1E, and 1F).
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The second patient was a 61-year-old man with metastatic renal cell carcinoma diagnosed in 1999. Right nephrectomy, bilateral pulmonary wedge resections, and a Whipple procedure for management of duodenal metastases were performed the following year. Treatment with a total of four cycles of interferon, interleukin-1, and 5-fluorouracil was administered with a complete response of approximately 17 months' duration. Follow-up imaging revealed new masses bilaterally. Radiofrequency ablation of an 8-mm nodule in the anterior portion of the left upper lobe was performed in December 2001. The patient returned that same month for radiofrequency ablation of a biopsy-proven 3.5 x 2.5 x 2.0 cm ellipsoid mass in the medial portion of the right lower lobe in conjunction with brachytherapy seed placement (Figs. 2A, 2B, and 2C).
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The third patient was a 65-year-old man with a history of locally advanced non-small cell lung carcinoma that was treated with pneumonectomy of the right lobe followed by Taxol-based adjuvant chemotherapy. A new 3.0 x 2.0 cm mass in the superior segment of the left lower lobe was identified on follow-up evaluation. This mass was treated with a combination of radiofrequency ablation and brachytherapy seed placement (Figs. 3A, 3B, 3C, and 3D).
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Technique
All three patients were treated under CT guidance. A cluster electrode
(Cool-Tip, Radionics, Burlington, MA) was used in the first patient for two
overlapping treatments; a 17-gauge, 2-cm active-tip cool-tip radiofrequency
electrode for six treatments in the second; and a 17-gauge, 3-cm active-tip
cool-tip radiofrequency electrode for three treatments in the third. The
radiofrequency generator (Cosman Coagulator-1, Radionics) was used with
maximum allowable output (101-149 W), and treatment times ranged from 1 to 12
min per placement. Local anesthesia was achieved with subcutaneous and
intradermal buffered lidocaine (1.5%). Four 180-cm2 grounding pads
were placed on the patients' thighs. All patients were consciously sedated
with IV midazolam (Versed, Abbott Laboratories, North Chicago, IL) and
fentanyl citrate (Sublimaze, Abbott Laboratories).
Brachytherapy began after completion of radiofrequency ablation in all three patients. In the first patient, two 10-cm-long 6-French vascular sheaths with a central 5-French needle (Ring biliary needle, Cook, Bloomington, IN) were inserted in the mass. The catheters were placed in the superior and inferior aspects of the mass, approximately 1.5 cm apart. Brachytherapy catheters were then inserted through the sheaths once the Ring biliary needle had been removed. Three-dimensional CT-based planning was used to deliver a single fraction dose of 16 Gy with a remotely afterloaded high-dose-rate 192Ir source to the tumor periphery (Figs. 1A, 1B, 1C, 1D, 1E, and 1F). In the second patient, a brachytherapy catheter was inserted into the inferior and anterior aspects of the tumor. Four permanent low-dose-rate 125I seeds were implanted along the needle tract as the needle was retracted under CT guidance. The brachytherapy catheter was then repositioned to three additional areas in the right lower lung mass depositing four seeds with each pass for a total of 16 implanted seeds. Total peripheral dose equaled 120 Gy (Figs. 2A, 2B, and 2C). Our third patient had treatment similar to the second with 12 low-dose-rate 125I seeds placed for a total peripheral dose of 144 Gy (Figs. 3A, 3B, 3C, and 3D).
Follow-Up
A chest radiograph was obtained 2 hr after the procedure in all three
patients to assess for pneumothorax. Interval follow-up CT images were
obtained, ranging from 1 to 12 months after the procedure.
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The first patient was observed in the recovery room for 2 hr before high-dose-rate brachytherapy and then for 1 hr after catheter removal. No pneumothorax was seen on the postprocedural CT images, and no complications (e.g., hemoptysis) occurred with brachytherapy. CT images obtained at 1-month follow-up revealed a nonenhancing mass measuring 3.0 cm with residual catheter tracts (Figs. 1A, 1B, 1C, 1D, 1E, and 1F).
The second patient did not develop a pneumothorax but did experience one short episode of hemoptysis during seed placement. A CT image obtained after the procedure showed a hazy peripheral density in the needle tract and adjacent parenchyma that was consistent with hemorrhage, which resolved without intervention. The patient was discharged after 2 hr of observation. Follow-up CT 12 months after radiofrequency ablation revealed a reduction in the size of the mass to 3.5 x 2.0 x 1.5 cm (Figs. 2A, 2B, and 2C).
A CT image obtained after the procedure in the third patient showed a small left apical pneumothorax. A chest radiograph obtained 2 hr after the procedure showed no interval change in the size of the pneumothorax. Follow-up radiographs obtained 1 day after radiofrequency ablation revealed a slight interval decrease in the size of the pneumothorax, which subsequently resolved. Follow-up imaging at 9 months revealed new metastatic nodules in the lung. However, tumor shrinkage (2.6 x 1.8 cm) was observed in the treated area (Figs. 3A, 3B, 3C, and 3D) with previously placed seeds now projecting over an aerated lung.
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Although fatal hemoptysis is a possible complication of interstitial brachytherapy [3, 4, 11], this conjunctive treatment proved to be safe in our patients, with the only side effects of a small pneumothorax and hemoptysis in two patients that resolved without intervention. Advantages of brachytherapy include well-defined distribution of radiation with rapid dose falloff and the ability to conform the dose in accordance to the target. This ability to conform the dose is further realized using afterloading catheters and high dose rates. High dose rate also offers the benefit of shortening overall treatment times—resulting in the capability to perform the procedures on an outpatient basis and decreasing the risk of seed displacement [3, 4]. Brachytherapy is more expensive than conventional external beam radiation therapy, but brachytherapy is more cost-effective because typically only one application as an outpatient procedure is required [3, 4]. Benefits of a minimally invasive technique such as radiofrequency ablation include reduced morbidity and mortality compared with surgery, lower cost, suitability for real-time imaging guidance, capability to be performed in an outpatient setting, and ability to create large regions of coagulative necrosis in a controlled setting [10].
Further arguments lend merit to the use of radiofrequency ablation in conjunction with brachytherapy in the treatment of inoperable localized lung tumors. The cytoreduction induced by radiofrequency ablation could decrease the number of clonogens that radiation would be required to control. Cell-cycle kinetics and the tumor microenvironment after radiofrequency ablation may also enhance the radiation effect, although we would not predict this benefit in the acute setting when radiation therapy is given as high-dose-rate brachytherapy. However, in the acute setting, the more classically described interactions between hyperthermia and radiation may be active [9]. Radiofrequency ablation in conjunction with brachytherapy has an increased capability to be performed in an outpatient setting and allows a higher degree of local control than radiofrequency ablation alone given the flexibility in delivery of different radiofrequency currents and conformation of brachytherapy doses. Although each modality has individually been shown to be effective in the treatment of lung malignancies, the potential synergistic effect of radiofrequency ablation and brachytherapy and the theoretic advantages elucidated earlier should be further evaluated as definitive therapy for inoperable localized lung tumors.
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