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Interventional Radiology |
1 Department of Radiology, "San Sebastiano" Caserta's Hospital, Via
F. Palasciano, Caserta 81100, Italy.
2 Department of Pneumology, "San Sebastiano" Caserta's Hospital,
Caserta 81100, Italy.
3 Department of Anesthesiology, "San Sebastiano" Caserta's Hospital,
Caserta 81100, Italy.
4 Department of Pathology, "San Sebastiano" Caserta's Hospital,
Caserta 81100, Italy.
Received December 19, 2003;
accepted after revision March 8, 2004.
Address correspondence to G. Belfiore, Via Caduti sul Lavoro n 55, Caserta
81100, Italy.
Abstract
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SUBJECTS AND METHODS. Thirty-three patients (26 men and seven women; age range, 44–75 years; mean age, 66 years) with unresectable malignant lung neoplasms underwent 35 CT-guided tumor ablation sessions. Follow-up CT was performed 6 months (29 cases) and 1 year (10 cases) after treatment. In 19 patients, these findings were correlated with cytohistopathologic assessment obtained with CT-guided fine-needle aspiration biopsy or core biopsy at 6-month follow-up. Size and CT appearance of the treated lesions were correlated with cytohistologic features and clinical scores.
RESULTS. Thirty-five technically successful radiofrequency ablation treatments were performed. The only complications in the periprocedural period were three cases of minor pneumothorax, five cases of sputum cruentum, and three asymptomatic pleural effusions. Contrast-enhanced CT performed at 6-month follow-up showed four cases of complete and 13 cases of partial lesion ablation, 11 cases of stabilized lesion size, and one case of increased lesion size. Contrast-enhanced CT performed at 1-year follow-up showed unchanged lesion size in six cases and reduction in four cases. Six-month cytohistologic examinations showed total coagulation necrosis in seven lesions and partial necrosis in 12. Clinical improvement in pretreatment symptoms was observed in 12 of 29 patients seen at 6-month follow-up. Eight patients died within 1 year of treatment of non–procedure-related causes.
CONCLUSION. Our experience suggests that radiofrequency ablation can be used successfully in unresectable lung cancer as an alternative or complementary treatment to radio- or chemotherapy. Larger studies are necessary to fully evaluate its potential combination with other treatment techniques.
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It is well known that for patients with stage I lung cancer, surgical resection is the treatment of choice, although some of these patients are ineligible for surgical intervention because of poor cardiopulmonary status or poor general health. Higher-stage inoperable lung tumors respond poorly to chemotherapy and radiotherapy regimens, and therefore, alternative treatment is desirable [4].
After animal studies proved the thermal effects of radiofrequency energy in lung tissue and its capability in the treatment of small pulmonary masses [11–13], radiofrequency tumor ablation began to be applied in the treatment of thoracic malignancies in humans [14–21]. The aim of this study was to evaluate the effectiveness, safety, technical feasibility, and complications of CT-guided tumor ablation with radiofrequency in the treatment of nonsurgical primary pulmonary malignancies as a possible alternative or complementary treatment to radio- or chemotherapy for palliation of the major symptoms of lung cancer (pain, cough, dyspnea). In addition, we sought to assess in vivo the effects of radiofrequency on the neoplastic tissue by performing fine-needle aspiration biopsy or core biopsy 6 months after the radiofrequency treatment.
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Our study included 21 cases of adenocarcinoma, 11 cases of squamous cell carcinoma, and one case of small cell carcinoma. None of the patients were candidates for surgery because of the stage of the tumor, comorbid medical or pulmonary dysfunction, or their refusal to undergo surgery. In 15 of the 33 patients, there were clinical or radiologic signs of active disease after radio- or chemotherapy. Briefly, we excluded patients with coagulation disorders, those with distant metastases, and those with involvement of the thoracic walls or massive invasion of the mediastinum but enrolled patients with tumors at any stage without regard to thoracic location.
Patients were divided into three groups on the basis of the tumor size: group 1 (n = 12), tumor diameter smaller than 3 cm; group 2 (n = 19), tumor diameter between 3 and 5 cm; and group 3 (n = 2), tumor diameter exceeding 5 cm. Patients were also stratified using a clinical scoring system developed ad hoc to measure pain, coughing, and dyspnea. We administered the test to determine this score before radiofrequency ablation and 6 months and 1 year after radiofrequency ablation (Table 1).
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Before treatment, we routinely used midazolam (0.04 mg/kg), tramadol hydrochloride (50 mg), and atropine (0.5 mg/kg) for premedication and sedation. In all patients, the usual set of coagulation parameters (platelet count and prothrombin time) was assessed. Immediately before the introduction of the targeting radiofrequency electrode, we used a local anesthetic cocktail containing Carbocaina (mepivacaine, AstraZeneca, 5–10 mL) and Naropin (ropivacaine hydrochloride, AstraZeneca, 4–5 mL). The electrode then was positioned. One of two medications was used for analgesia. Seventeen patients received IV remifentanil (0.06 mg/kg/min), whereas 16 patients received Sevorane (sevoflurane, Abbott Laboratories) mixed with air (4%) and oxygen (50%) administered with a facial mask during spontaneous breathing until a minimum alveolar concentration of 0.8 was obtained. During the treatment, patients underwent continuous pulse oximetry and ECG. Arterial blood pressure was checked every 7 min.
A contrast-enhanced CT scan (baseline) was obtained before radiofrequency
ablation to identify the target lesion and to determine the optimal electrode
placement in the same manner as in a CT-guided fine-needle aspiration biopsy.
In 23 cases, we used a radiofrequency system applicator with a 17-gauge cold
needle, internally cooled by infusion of 0°C saline and tipped with a
single or cluster electrode, and a 200-W radiofrequency generator (Cosman
Coagulator-1, Radionics). In 19 cases, we used a cool-tip single electrode. In
four of these procedures, multiple repositionings (maximum number, two) of the
needle in different regions of the tumor were required to ensure ablation of
the entire lesion. In four other cases, we inserted a cluster electrode into
lesions (all, 
3 cm), with no repositioning required. In the remaining 10
cases, the radiofrequency ablation treatment was performed by single
positioning of a 15-gauge multitined expandable electrode with a
radiofrequency generator 1500X (StarBurst-compatible, RITA Medical
Systems).
With both systems, the target tissue temperature was 90–95°C, as measured by a specific device in the radiofrequency generator that provided a continuous display of the temperature throughout the procedure. Once the target temperature was achieved, the radiofrequency energy deployment was continued for 9–12 min in all cases. Grounding was achieved using dispersive pads placed on the patient's upper thighs.
Contrast-enhanced CT was performed immediately after the tumor ablation procedure, and then 1 week, 1 month, 6 months (29 cases), and 1 year (10 cases) after treatment. In 19 patients, the follow-up CT findings (tumor size and appearance) were correlated with the cytohistologic features obtained by CT-guided fine-needle aspiration biopsy or core biopsy at 6 months and 1 year after treatment (Table 1).
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In most cases, contrast-enhanced CT scans obtained immediately and 1 week after radiofrequency ablation showed a nonenhancing central area with decreased density (ablation zone), with intralesional bubbles and enveloped ground-glass opacity surrounding the tumor (Figs. 1A, 1B, 1C, 1D and 2A, 2B, 2C).
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As illustrated in Table 1, by 6 months after treatment, four patients (three from group 2 and one from group 3) died of causes unrelated to the procedure. Two patients died of hepatic failure due to liver cirrhosis, one died of heart failure, and one died of massive extrathoracic tumor growth.
Contrast-enhanced CT findings of the remaining 29 cases showed that the size of the ablation zone had not changed (Fig. 1A, 1B, 1C, 1D) in 11 cases (38%; three patients [25%] in group 1 and eight [50%] in group 2). The size of the ablation zone had been reduced in 17 cases (59%; nine patients [75%] in group 1, seven [48%] in group 2, and one [100%] in group 3); four (23%) of the 17 actually showed a complete ablation (i.e., nearly total disappearance of the mass) (Figs. 2A, 2B, 2C and 3A, 3B). In the one remaining patient (3% of total patients treated), an increase in neoplastic tissue (original tumor size, 4.4 cm) was observed.
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By 1 year after treatment, four more patients had died (one from hepatic failure, one from heart failure, and two from massive extrathoracic tumor growth) and seven others were lost to follow-up. Thus 18 patients were contacted for the clinical–radiologic evaluation, but only 10 were available to undergo contrast-enhanced CT. Findings of the CT study showed unchanged lesion size in six patients (two from group 1, three from group 2, and one from group 3) and a further reduction of the ablation zone in the remaining four patients (three from group 1 and one from group 2) (Figs. 4A, 4B and 5A, 5B, 5C, 5D) compared with the findings on the 6-month CT scan.
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In 19 of the 29 cases, the contrast-enhanced CT scans obtained at 6-month follow-up were correlated with the cytologic and histopathologic examinations (Table 1). In the biopsy specimens, a pattern of total substitution with coagulation necrosis was observed in seven cases (36%; five from group 1 and two from group 2); a pattern of partial substitution (mixed pattern of solid and necrotic tissue) was reported in 12 cases (63%; 11 from group 2 and one from group 3) (Figs. 1A, 1B, 1C, 1D and 5A, 5B, 5C, 5D).
As for the group analysis, in the 12 patients from group 1, tumor size on 6-month CT was unchanged in 25% and was reduced in 75%; in three patients, the lesion had almost completely disappeared. Biopsy was not considered safe for the three patients with a "vanishing" lesion and was refused by four other patients; in the remaining five patients, complete necrosis in the biopsy specimen was observed. Among the 16 surviving patients from group 2 at 6-month follow-up, the tumor size was reduced in 48% (one patient had a vanishing lesion), unchanged in 50%, and larger in one patient. At biopsy, two cases with patterns of complete necrosis and 11 with patterns of partial necrosis were reported. In the remaining patient from group 3 who was alive at 6-month follow-up, CT showed reduction in tumor size and biopsy showed partial necrosis.
The clinical results are shown in Tables 1 and 2. Thoracic pain was completely resolved in five patients, partially reduced in four, and slightly increased in two. In seven patients, a reduction of coughing was observed, and six patients reported better respiratory performance, although no corresponding improvement of laboratory findings (oxygen pressure and oxygen saturation values) was seen. Thus, as shown in Table 2, at 6-month follow-up, the ratios between the sum of clinical points and the number of patients decreased from 1.73 to 1.38 for pain scores, from 1.45 to 1.17 for coughing scores, and from 1.48 to 1.14 for dyspnea scores, indicating that good palliation was achieved.
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At 1-year follow-up, clinical evaluation was available for 10 patients that showed a trend for decrease in pain (three patients) and for worsening of coughing and dyspnea (two patients); the corresponding ratios showed mild further decrease for pain scores and increase for coughing and dyspnea scores (Table 2). No clear correlation was evident between radiologic response and clinical improvement: 53% (8/15) of patients with decreased lesion size on CT actually had unchanged clinical patterns, and 38% (5/13) with unchanged lesion size on CT showed clinical improvement at 6-month follow-up.
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Radiofrequency tumor ablation has become a credible addition to the arsenal of minimally invasive cancer therapies with palliative goals. The technique is based on the premise that local disease control can have a positive effect on survival or quality of life in selected populations [24]. Indeed, patients with inoperable disease may have the chance to obtain satisfactory palliation by inducing a consistent zone of tumor necrosis without the added complications of a surgical procedure that requires general anesthesia, chest tube drainage, and prolonged hospitalization [25]. This study evaluated the feasibility of an innovative therapy to offer these patients an effective palliative alternative. The procedure is technically simple and similar to the fine-needle aspiration biopsy technique that we use routinely [26]. Treatment time averages 60 min both in our patients and in those reported by other authors [27].
MacGahan et al. [28] first used radiofrequency ablation for hepatic neoplasms in an animal model. The technique was then effectively used for primary and recurrent liver tumors with some satisfactory clinical results [29]. The effects of radiofrequency ablation for normal lung tissue or lung tumors in animals and humans were also reported [11, 14, 30, 31]. Radiofrequency ablative therapies deliver AC into the tissue to destroy tumor cells by increasing the temperature until coagulation necrosis occurs [29, 32]. We used cytohistopathology to verify the effects of radiofrequency ablation on lung tumors: after 6 months, these lesions retained a total coagulative necrotic pattern in seven of 19 cases and a mixed necrotic pattern with viable neoplastic cells in 12 cases. In our experience with the technique, the so-called heat sink effect has not reduced its effectiveness. Even lesions located close to major vessels responded well to the treatment (Fig. 4A, 4B). Lung tumors seem well suited to radiofrequency treatment because the surrounding air in the adjacent normal lung parenchyma provides insulation that may concentrate radiofrequency energy [4, 12]. In fact, in postoperative CT scans, we observed an inhomogeneous intralesional area (white zone) of bubble-like coagulation (Fig. 2A, 2B, 2C) and edema induced by heat.
Few reports in the literature have described the survival rates of patients treated with radiofrequency ablation [20, 27]. In our series, at 6-month follow-up, the patients from group 1 showed the highest percentage of complete ablation and size reduction on CT, in addition to 100% (5/5 patients) total necrotic patterns in biopsy specimens. In group 2, tumor size on CT decreased in approximately 50% of the cases; two cases showed patterns of complete necrosis and 11 showed patterns of partial necrosis. The one patient from group 3 alive at 6 months showed tumor size reduction on CT and a pattern of partial necrosis. On 1-year follow-up CT (10 patients total), group 1 showed stable lesions (two patients) or further decrease in lesion size (three patients), whereas group 2 showed stable lesions (three patients) and further decrease in tumor size (in one patient). The group 3 patient was also stable. Therefore, it appears that smaller lesions tend to respond better to radiofrequency ablation, as has also been reported by others [21], showing size reduction [19], total cytoreductive effect, and, possibly, higher patient survival rates.
From our experience in this preliminary study, we speculate that the use of CT appearance of lung nodules after radiofrequency ablation as the only criterion for complete necrosis and success of therapy may not be sufficient. In fact, although the histopathologic examination of treated zones is prone to false-negative findings, some neoplastic cells were observed in the aspirates from low-density zones in our biopsy specimens, even in 42% (5/12) of the cases with reduced tumor size on CT at 6 months. We then stress the need to check the evolution of treated nodules with CT-guided histopathologic examination together with the CT findings.
Early experience showed that thermal ablation by means of laser or radiofrequency energy could reliably create foci of tissue necrosis of up to approximately 1.6 cm in diameter. However, because most tumors are larger than that by the time they are detected, successful treatment has, until recently, necessitated the use of either multitreatment electrodes, multiple treatment sessions, or both. [33]. For this reason, of 19 tumors exceeding 3.5 cm, we treated four with double repeated radiofrequency electrodes in the same session and also re-treated one at 3 and 6 months after ablation to ensure, if cytology revealed a mixed pattern, the complete ablation of residual tumor cells. Treatment tolerability was also taken in consideration.
As for complications, we had similar results with both radiofrequency types of electrodes, with only a few periprocedural occurrences and with no delayed complications. With the described protocol, we also treated lesions localized in particular regions adjacent to large vessels, spine, and scapula that were considered risky or difficult to approach [27], but we encountered no adverse effects. We believe that this kind of treatment requires a great deal of operator experience [26] and close cooperation with the anesthesiologists to ensure the shortest treatment time as well as the shortest recovery time; in this respect, the patients who received IV remifentanil hydrochloride experienced less discomfort than those sedated with sevoflurane.
Our clinical scoring system is not a validated instrument for quality-of-life measurements and was only created, as has systems by others [16], to give an idea of the trend of the clinical evolution in these patients. Twenty-two (76%) of 29 patients with pain, cough, and dyspnea reported some improvement in their symptoms using this scoring system at 6-month follow-up compared with the baseline clinical pattern. As previous authors have stressed, it is important to consider the patient's quality of life after a therapeutic procedure [34, 35].
In agreement with the experience reported by others [12, 16, 24, 25], our experience suggests that the radiofrequency ablation therapy can be successfully used as an alternative or complementary treatment for unresectable lung cancer. In addition, the quality of life of some patients can be improved. Radiofrequency ablation is a local, minimally invasive treatment that, compared with surgery, provides us with a chance to reduce some damage to the lung parenchyma and to avoid systemic effects to the patient's general health. Other possible advantages are the anticipated reduction in morbidity and mortality, low cost, and short hospital stays (average, 2–3 days).
In our study, we obtained a good response in smaller lesions (< 3 cm); the hypothesis that radiofrequency ablation may be offered as the best therapeutic alternative to nonsurgical candidates with small, non–oat cell lung tumors should be evaluated in large and long-term studies. As for the larger tumors, we speculate that the only rationale for treatment is palliation of local symptoms to obtain a subtotal cytoreductive effect before radio- or chemotherapy.
The long-term clinical benefits of radiofrequency ablation for the treatment of malignant tumors still remain to be proven, and improvements in radiofrequency equipment, ablation techniques [32], and even imaging follow-up procedures may be made. However, the extensive laboratory and animal experience, in combination with the results of preliminary clinical studies, suggests that this technique may play an important role in the treatment of patients with primary and secondary lung tumors, and the optimal combination of radiofrequency ablation with chemotherapy and radiotherapy protocols should be addressed in future studies.
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