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Original Report |
1 Department of Radiology, Hull and East Yorkshire Hospitals NHS Trust, Anlaby
Rd., Kingston Upon Hull, HU3 2JZ, United Kingdom.
2 Department of Urology, Hull and East Yorkshire Hospitals NHS Trust, Kingston
Upon Hull, HU3 2JZ, United Kingdom.
3 Present address: Department of Radiology, Southampton University Hospitals NHS
Trust, Tremona Rd., Southampton, SO16 6YD, United Kingdom.
Received May 20, 2002;
accepted after revision August 28, 2002.
Address correspondence to D. J. Breen.
Abstract
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CONCLUSION. Early experience suggests that radiofrequency ablation is a safe, well-tolerated, and minimally invasive therapy for patients with solid renal masses. In the era of nephron-sparing surgery, radiofrequency ablation may have a role in the management of small problematic renal masses.
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Radiofrequency ablation is a technique by which heat induced by focused monopolar electrocautery produces a sphere of coagulative necrosis. This technique has been used successfully in the ablation of solid liver tumors [8, 9]. Renal radiofrequency ablation has been described in an experimental rabbit model [10], preoperatively [11], intraoperatively before surgical excision [12], and in patients with von Hippel-Lindau disease [13]. The purpose of our study was to assess the safety and efficacy of percutaneous radiofrequency ablation of small renal masses with medium-term imaging and clinical follow-up.
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We performed 14 radiofrequency ablation sessions (each 12-min treatment application was defined as a session) during 11 treatment sittings (each admission counted as a sitting) for 11 lesions in eight patients. The patients included six men and two women, ranging in age from 60 to 88 years (mean age, 73.4 years).
Diagnosis of a solid renal lesion as renal cell carcinoma was based on needle biopsy results (n = 3) or the established CT criteria (n = 8), including average density greater than 20 H, enhancement of more than 20 H after contrast administration [14] with or without additional criteria such as absence of fat and contour deformation [1]. Four of these 11 masses also had shown growth during a prior period of observation.
Patients were admitted the day before the procedure, and baseline biochemical and clotting studies were performed. The masses were between 1.5 and 5.5 cm (mean, 3.0 cm), and all were staged as T1 N0 M0 according to the 1997 TNM classification [3] of imaging criteria. Two masses were central with contact with the renal sinus, and nine were exophytic [7] (Fig. 1A, 1B). Indications were imperative (single functioning kidney) in two patients and elective (normal contralateral kidney) in six patients.
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The procedure was performed under imaging guidance, either with sonography (Sonoline Elegra, Siemens, Seattle, WA) (n = 8) or CT fluoroscopy (Somaton Plus 4, Siemens, Forcheim, Germany) (n = 5) with the patients in the prone position. Before the procedure, each patient was administered a single-dose IV antibiotic prophylaxis with metronidazole and cefuroxime. In 10 of 11 sittings, conscious sedation was used (midazolam and fentanyl citrate) in incremental doses with local anesthetic (lignocaine 1%). Patients were monitored by a trained interventional nurse throughout the procedure. One patient with von Hippel-Lindau disease had three upper pole tumors ablated in one sitting under a general anesthetic.
A water-cooled radiofrequency ablation system was used. The technique has been described before [8, 9, 13]. All procedures were performed by a single operator. Either a single 18-gauge (n = 3) or a cluster (n = 10) Cool-tip probe (Radionics, Burlington, MA) was placed into the lesion under imaging guidance (Fig. 2B). Four grounding pads were attached to the patient's thigh. Impedance-regulated radiofrequency energy from a generator at 150–200 W was applied in 12-min aliquots. Baseline impedance was not recorded, but it was approximately 60–80 µ. We monitored probe temperatures by a thermocouple and tissue impedance through in-built circuitry. An iced saline perfusate (1–3 L at 0°C) was used to cool the probe tip and was driven by a peristaltic pump (Radionics/Watson-Marlow, Medford, MA) to maintain a tip temperature of 10–15°C. A minimum target temperature of 60°C was used. The generator was set on an automatic impedance cutoff mode that stopped energy delivery if impedance increased by more than 20 µ above baseline to prevent tissue charring or boiling.
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At the conclusion of the procedure, the maximum tip temperature and the 1-min cooldown temperature were noted as indicators of heat deposition. If a different area of the tumor needed ablation, a second 12-min treatment was performed with the probe repositioned.
After the procedure, patients were monitored in the recovery area for 2 hr before being returned to the ward for overnight observation. Routine clinical and biochemical checks were made. CT was performed 72 hr after the procedure. Unenhanced arterial (25 sec) and nephrographic (90 sec) scanning was performed at 5-mm collimation, with or without delayed (3-min) scanning. Complete lack of enhancement at the site of the tumor was taken as the end point of successful treatment.
Subsequent follow-up was clinical (approximately every 6 months), biochemical (serum creatinine level), and radiologic. CT was performed every 3 months for 6 months and every 6 months thereafter. After the first year, only nephrographic phase scanning was performed.
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CT performed 3 days after treatment revealed complete ablation with no
residual enhancement in nine of the 11 masses in our series. One mass
measuring 3.5 cm in diameter was adequately ablated with one 12-min session,
although a second 12-min aliquot was used for two larger masses (one measuring
3.7 cm and the other, 5.5 cm). Two lesions showed asymmetric marginal
enhancement of residual tumor of less than 10%
(Fig. 3B) and were further
treated under CT guidance at a later date. No lesion needed more than two
treatment sessions. In four lesions, an area of increased density
(Fig. 2C) representing
hemorrhage and necrosis was seen on the unenhanced scan after radiofrequency
ablation. One patient had an intrarenal vessel coursing along the margin of
the ablated lesion (Figs. 4B
and 4C) that remained
unchanged on follow-up imaging (Fig.
4D). Seven of the eight patients showed no evidence of recurrence
on follow-up (range, 10–26 months; mean, 17.1 months). On follow-up
imaging, we noted a reduction in the volume of the ablated, coagulated
nonenhancing mass (range, 0–4 cm; mean, 1.9
cm).
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One patient with a 3-cm exophytic mass in the lower pole had asymptomatic thermal injury to the ipsilateral psoas major and quadratus lumborum muscles (Fig. 5). Another patient had a small segmental infarction in the path of the probe after treatment of a renal sinus lesion in a solitary kidney (Fig. 4C). A slight increase in creatinine levels (0.8–1.5 mg/dL) was noted during the follow-up period. Slightly reduced cortical attenuation suggestive of local infarction was seen in one patient adjacent to the treated area after retreatment of a residual enhancing mass, with no change in serum creatinine level on follow-up (Fig. 3D). The mean serum creatinine level before treatment was 1 mg/dL and after the procedure, 1.1 mg/dL. No significant rise in creatinine level was noted in seven of the eight patients during follow-up (range, –0.3 to 0.7 mg/dL; mean rise, 0 mg/dL).
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One patient with satisfactory findings on imaging after radiofrequency ablation died during follow-up. The cause of death was stone-related severe biliary sepsis and cholangitis that developed after a cholecystectomy was performed 18 months after the ablation; no evidence of recurrent tumor was found on CT follow-up at the time of surgery. One patient with von Hippel-Lindau disease who had previously undergone nephrectomy had four tumors treated during two sittings. During the last follow-up CT, these ablated areas remained unenhanced, but two separate metachronous nodules of enhancement were noted. The disease progressed rapidly, and the patient died from metastatic renal carcinoma within 3 months. Two large tumors were identified at autopsy, both centered around the mid polar region. These tumors engulfed both poles (the site of previous ablation); thus, it was not possible to exclude recurrence from the previously ablated site. This patient's creatinine level had steadily increased from 1.4 to 2.9 mg/dL. Her case has been included here as a treatment failure.
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As populations age, conservation of renal tissue is a desirable goal. Ongoing diseases and conditions such as diabetes, hypertension, nephrotoxic chemotherapy, and vascular disease can damage renal parenchyma [17]. Bilateral renal tumors occur in 3–5% of patients presenting with renal cell carcinoma [1, 17], which further highlights the need for renal conservation. Bilateral nephrectomy (in the presence of imperative indications) usually results in poor quality of life because of the need for dialysis, particularly when associated with comorbid disease [18]. The fact that approximately 10% of excised small renal tumors are benign [1, 5] further reinforces the need for less radical interventions. The main argument against nephron-sparing surgery is the high (18%) reported incidence of tumor multicentricity [6]. However, clinically relevant multicentricity is thought to be between 5% and 10%, because actual incidence of tumor recurrence is much lower than would be otherwise predicted [5]. Thus, the role of nephron-sparing interventions is firmly established in the setting of localized renal carcinoma.
Partial nephrectomy or nephron-sparing surgery, although well tolerated, remains a technically demanding procedure [6]. Complication rates between 12% and 20% have been reported [7, 16], and the rate is slightly worse in the group for whom surgery is imperative and those with central tumors [7]. In a series of 76 patients, eight patients had hemorrhagic complications, four of which needed selective embolization [9]. Other complications include false aneurysm, anteriocaliceal fistula, and renal arterial thrombosis [4]. The desire to avoid such complications has led to the emergence of relatively noninvasive techniques, including laparoscopic partial nephrectomy, laparoscopic renal cryoablation, focused sonography, and laser-induced necrosis [19].
In our small series of 11 ablated masses, no significant complications occurred. All patients were fit to be discharged within 24 hr. It is our belief that renal radiofrequency ablation will make its niche among these minimally invasive renal conservation interventions for the treatment of localized renal carcinoma. The kidney is particularly suited to radiofrequency ablation because it is anatomically separate in the retroperitoneum, malignancy is usually unifocal (contrary to the prostate) [19], and the surrounding perirenal fat may help prevent dissipation of the applied heat during the procedure [20].
Few authors have reported their early experience with renal radiofrequency ablation both in the experimental and in vivo setting. Zlotta et al. [11] ablated three tumors before resection, and the pathologic specimens showed complete tumor necrosis. Walther et al. [12] ablated nine tumors in four patients at surgery using intraoperative sonography; 10 of 11 tumors were deemed to have a complete treatment, and the remaining tumor showed 35% necrosis. Pavlovich et al. [21] recently published their results with 24 tumors of less than 3 cm in 21 patients, 19 of whom had von Hippel-Lindau disease. They used a 50-W, 460-kHz generator and a noncooled coaxial probe system with temperature sensors designed to monitor treatment temperature at the periphery of the lesion. No major complications were reported, and 79% of the tumors ceased to enhance at the first 2-month follow-up. These authors mention the lack of long-term follow-up data on these treated lesions as a limitation of their study. Gervais et al. [13] treated nine tumors in eight patients during 24 sessions, with a mean follow-up of 7 months; three tumors in their series were larger than 3 cm. Two of these larger tumors required multiple sittings; persisting enhancing tumor tissue needed multiple ablative procedures.
We treated 11 masses in eight patients with a mean follow-up of 17 months. Seven of the eight patients remain free of tumors. One patient in our series had bilateral multiple aggressive renal tumors and left nephrectomy and underwent multiple ablative procedures on the contralateral kidney. Although the treated masses remained nonenhancing on available follow-up, this patient died of metastatic renal carcinoma. On her last follow-up CT, two metachronous nodules were noted in an untreated area. These tumors rapidly increased in size, and at pathology they were found to envelope almost the entire kidney. Therefore, it was difficult to exclude recurrence in a treated area. At the time she gave consent for multiple ablations, this patient resisted an offer of nephrectomy and lifelong dialysis. With hindsight, we think she might have been better served by a radical nephrectomy, but given the aggressive nature of the cancer, it is doubtful that any survival advantage would have been gained. Nevertheless, for the purpose of this study, we have included her as a treatment failure.
Radiopathologic correlation in both experimental and clinical studies has shown that imaging findings predict the region of coagulation necrosis within 2 mm [9]. Masses larger than 3 cm in our series required two 12-min aliquots of ablation to ensure complete necrosis. Imaging after radiofrequency ablation is critical. We routinely performed arterial phase (25 sec), nephrographic phase (90 sec), and delayed (3 min) CT 3 days after radiofrequency ablation. Imaging earlier than this is not predictive of the true diameter of coagulation necrosis, as has been shown in liver radiofrequency ablation [8, 9]. Increased density on the unenhanced scan signifies radiofrequency ablation hemorrhagic necrosis (Fig. 2C) and was seen in four of our eight patients. Any asymmetric enhancement on the arterial or nephrographic phase images implies residual tumor (Fig. 3B) and calls for further treatment. A nearby vessel can mimic residual tumor (Fig. 4B), but early interval scanning helps to differentiate this finding from true tumor recurrence. Presence of a vessel may also act as a local "heat sink" [13] and cause incomplete tumor ablation, particularly for central tumors. Close attention should also be paid to collateral damage (Figs. 4C and 5), particularly to the bowel. Clinical observation for 24 hr after the procedure is vital, particularly for pedunculated anterior lesions. A rigid follow-up schedule is desirable to diagnose and treat any residual or recurrent disease. Such follow-up requires close collaboration of the radiologist with the urologist and considerable radiologist time for clinical management, organization of follow-up, and frequent image review [22].
During radiofrequency ablation, current alternates at 200–1200 KHz radiofrequency, resulting in ionic agitation around the monopolar probe tip [15, 23]. This agitation causes heat, inducing tissue necrosis. The degree of tissue necrosis (and the diameter) depends on the energy deposited and the rate of cooling (via conduction and perfusion) and is modified by tissue interactions [9, 23]. Between 60° and 100°C, instantaneous cell death occurs from protein denaturation. At higher temperatures, vaporization, boiling, and tissue charring occur, increasing impedance and reducing heat dissipation and thereby resulting in a smaller area of necrosis. A probe with a lower tip temperature therefore induces a greater volume of tissue necrosis.
We used a standard 15-cm cluster probe for all but two small tumors during each 12-min application. The modality for imaging guidance was chosen so as to provide adequate lesion visualization. Although adequate positioning can be obtained using either sonography or CT, gaseous microbubbles produced by the procedure preclude adequate sonographic visualization of the lesion's outline during ablation [23]. CT was preferentially used for retreatment of viable crescents of tumor or when the lesion was poorly visualized on sonography.
In line with current thinking, we used the established CT criteria of a base density of greater than 20 H, enhancement greater than 20 H, and absence of fat with or without contour deformation to characterize small renal masses [1, 14]. Histologic confirmation to exclude metastasis was obtained in only three of 11 masses in patients with known history of extrarenal malignancy. In addition, four masses showed growth during a prior period of observation. Studies have shown repeatedly that the imaging diagnosis of solitary renal mass is more accurate than cytologic analysis of fine-needle aspirate or histologic analysis of core biopsy specimens [1, 24] and has a specificity exceeding 85% [14]. In a study that compared histologic analysis of intraoperatively obtained core-needle biopsy specimens with histologic evaluation of the surgical specimen, a false-positive rate of 34% and a false-negative rate of 20% were noted. [25]. Furthermore, studies have shown that needle-track seeding can occur after biopsy [25].
One disadvantage of radiofrequency ablation is lack of pathologic material for the purposes of tumor grading or staging. This lack of information might interfere with subsequent determination of prognosis or surveillance programs [4].
The particular limitation of our study is its small sample size. But this study represents our early experience and, with a mean follow-up of 17.1 months, gives insight into medium-term outcome of renal radiofrequency ablation. Having established the safety of this procedure, we are optimistic about the role of radiofrequency ablation and hope to extend the scope of radiofrequency ablation as an elective alternative to nephronsparing surgery in small renal tumors.
The decision whether or not to treat a small or incidentally detected renal neoplasm should be made with a balanced multidisciplinary approach that takes clinical and comorbidity factors into account. The issue of lead-time bias with earlier detection has been raised [26]. Several solid lesions being followed by Bosniak et al. [27] have shown little change on long-term follow-up and therefore seem unlikely to affect the longevity of the patient. However, a compelling logic to intervene exists when a lesion is small, confined to the kidney, and is likely to be of lower grade. The prognosis of metastatic cancer is poor, with 50% mortality at 6 months [28]. Small incidentally detected tumors do grow and even metastasize, the incidence being as high as 7% in tumors smaller than 3 cm [29]. For a tumor to reach 3 cm requires approximately 30 doublings and development of neovascularity [30]. In one study, 24 of the 40 tumors being followed needed surgery over their total follow-up period of 12 years [27]. However, it remains impossible to predict which tumor is going to affect the longevity of the patient because prognosis depends on both the grade of the tumor and the host response [31].
This debate regarding the clinical significance of small incidentally detected lesions has largely been driven by an acknowledgement that radical and even nephron-sparing surgery carries its own not insignificant morbidity. The decision-making process can be helped by the findings of long-term follow-up studies [27, 30, 31], which have shown that small renal tumors grow, on average, 3 mm a year and that tumors larger than 4.5 cm are of higher grade and frequently metastasize. The clinical decision to treat is much less onerous when a low morbidity, minimally invasive, and nephron-sparing technique such as radiofrequency ablation represents a real therapeutic option.
In conclusion, several advances have been made in the field of nephron-sparing interventions for the treatment of small renal masses. Percutaneous radiofrequency ablation appears to be a safe and effective alternative that preserves the remaining ipsilateral parenchyma. Such advances are likely to improve the prospect of long-term survival in patients with renal cell carcinoma, for which no satisfactory treatment exists once the tumor has metastasized. Further work needs to be done in establishing the radiopathologic correlates after radiofrequency ablation before the technique is established as a genuine alternative to nephron-sparing surgery for small renal tumors.
Acknowledgments
We thank Alison Vickers for her invaluable secretarial work, including
organizing follow-up imaging, gathering patient records, and preparing the
manuscript; and G. H. Urwin and D. J. Almond for clinical follow-up and
allowing us to report on their patients.
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pathologic findings. AJR
1994:163:597
–605 3.0 cm) renal parenchymal tumor:
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