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Original Research |
1 Radiology Department, Vimercate General Hospital, Via Cesare Battisti 23,
20059 Vimercate, Milan, Italy.
2 Department of Radiology, Cattinara Hospital, University of Trieste, Trieste,
Italy.
3 Department of Diagnostic Radiology, University Milano-Bicocca, Hospital San
Gerardo, Monza, Milan, Italy.
4 Infectious and Tropical Diseases Division, Istituto Di Ricovero e Cura a
Carattere Scientifico (IRCCS), San Matteo–University of Pavia, Pavia,
Italy..
Received September 30, 2007;
accepted after revision May 5, 2008.
Address correspondence to M. F. Meloni
(francameloni{at}yahoo.it)
Abstract
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MATERIALS AND METHODS. Twenty-nine patients with 30 renal tumors (18 men, 11 women; mean age, 73 years; range, 53–83 years) underwent percutaneous radiofrequency ablation at a single center between March 1998 and January 2007. The imaging follow-up schedule was both contrast-enhanced sonography and CT or MRI 4 months after completion of treatment and every 4 months for the first year. Thereafter, the follow-up schedule was contrast-enhanced sonography every 4 months with CT or MRI every 8 months. The chisquare test with Yates correction was used to evaluate positive and negative predictive values and accuracy.
RESULTS. One patient was scheduled to undergo surgical resection, and another patient was lost to follow-up. Twenty-seven patients with 28 renal tumors participated in follow-up. The concordance between contrast-enhanced sonographic and CT or MRI findings was 100% for 27 of 28 tumors (96.4%) that had a hypervascular pattern before treatment. In the case of the tumor that was hypovascular at imaging performed before percutaneous radiofrequency ablation, local tumor progression was missed at contrast-enhanced sonography. The sensitivity, specificity, positive predictive value, negative predictive value, and overall accuracy of contrast-enhanced sonography were 96.6%, 100%, 100%, 95.8%, and 98.1%.
CONCLUSION. Contrast-enhanced sonography is an effective alternative to CT and MRI in the follow-up of renal tumors managed with percutaneous radiofrequency ablation.
Keywords: contrast-enhanced sonography • follow-up • intervention • kidney • neoplasms • radiofrequency ablation
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Sonographic contrast agents consisting of non-air-filled microbubbles have become available. The effect of these agents is based not on rupture of the microbubbles but on the continuous resonance of the microbubbles in a low-mechanical-index sonographic field. This mechanism of enhancement allows real-time imaging of the microcirculation. The aim of this retrospective study was to assess, with contrast-enhanced CT or MRI as the reference imaging technique, the diagnostic performance of low-mechanical-index contrast-enhanced sonography in the detection of local tumor progression after percutaneous radiofrequency ablation of renal tumors.
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Imaging
CT and MRI—Because newer generations of CT scanners became
available, contrast-enhanced CT was performed until 2000 and MDCT thereafter.
Because patients were referred for radiofrequency ablation from other
institutions, CT and MRI before treatment and during follow-up were performed
with several types of equipment. All examinations were performed before and
after IV administration of contrast material, and imaging findings were
evaluated for tumor staging according to well-established criteria
[6,
11]. Briefly, the diagnostic
criteria were a mass causing the renal contour to bulge and attenuation or
signal intensity different from that of normal renal parenchyma; presence of
necrotic changes; uneven margin or pseudocapsulation; venous extension;
metastasis; lymphadenopathy; and adjacent organ invasion. A central stellate
scar in an otherwise homogeneously enhancing lesion can suggest oncocytoma.
Identification of fat allows the diagnosis of angiomyolipoma. The best
diagnostic accuracy at CT is obtained during the nephrographic phase.
Hard copies of CT scans and MR images were retrospectively interpreted by two independent senior radiologists with 15 and 20 years of experience in renal imaging who were blinded to the results of contrast-enhanced sonography. The two independent senior radiologists were from different institutions, and the assessments were made at their institutions.
Contrast-enhanced sonography—All sonographic studies were performed with units equip ped with software for contrast media. The sono graphic equipment used in this study is listed in Table 1. Contrast-enhanced sonography was per formed with a sulfur hexafluoride–filled micro bubble contrast agent (SonoVue, Bracco) licensed for use in abdominal and vascular imaging in most European countries. A bolus of a standard dose of 2.4 mL of the contrast agent through a 20-gauge cannula followed by a 10-mL normal saline flush was injected into an antecu bital vein. Contrast-enhanced sonography was performed at a low pressure setting that was automatically defined with the contrast media software of the sono graphic equipment.
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Preprocedural contrast-enhanced sonographic studies were correlated with outside CT or MRI studies. All contrast-enhanced sonographic studies obtained before radiofrequency ablation, the day after treatment, and during follow-up were performed by the same radiologist, who had 5 years of experience in contrast-enhanced sonography. The images were stored on digital videodisks for further analysis. The reader was blinded to CT and MRI findings. Tumor size, location (central or peripheral), and enhancement characteristics were evaluated.
Renal tumors were defined as hypervascular on contrast-enhanced sonograms when they displayed homogeneous or heterogeneous distribution of echo intensity brighter than the adjacent renal parenchyma during the arterial corticomedullary phase (15–20 seconds after microbubble injection). Tumor washout was generally faster than that of normal renal parenchyma, so the lesion appeared relatively hypoechoic to kidney starting 30–40 seconds after injection. Renal tumors were defined as hypovascular on contrast-enhanced sonograms when they had scarce enhancement and thus lower echogenicity with respect to adjacent renal parenchyma both in the corticomedullary phase and in the late phase.
The day after treatment, readers of both contrast-enhanced sonograms and CT scans or MR images were asked to check for evidence of complications of radiofrequency ablation or the persistence of disease, presenting as viable enhancing foci within the tumor. Tumor progres sion was assessed during follow-up. Radiofrequency ablation was considered successful at imaging when there was no enhancement in the case of hypervascular renal tumor or no increase in size in the case of hypovascular tumor (Fig. 1A, 1B, 1C, 1D, 1E, 1F).
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Follow-Up
Follow-up was performed with CT or MRI and with contrast-enhanced
sonography. Initial posttreatment scans were obtained 1 day after
radio-frequency ablation. When residual tumor was identified on initial
posttreatment images, a second session of radiofrequency ablation was
scheduled. Follow-up imaging with CT or MRI and with contrast-enhanced
sonography was scheduled to take place 4 months after completion of treatment
and every 4 months for the first year. Subsequent follow-up was scheduled to
take place every 4 months with contrast-enhanced sonography and every 8 months
with CT or MRI.
Statistical Analysis
The chi-square test with Yates correction was used to evaluate positive and
negative predictive values and accuracy. A value of p < 0.05 was
considered to indicate a statistically significant difference.
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Before treatment, CT or MRI showed that 28 of 30 tumors (93.3%) were hypervascular and two of 30 tumors (6.7%) were hypovascular. Twenty-one of 23 tumors (91.3%) had a hypervascular pattern at contrast-enhanced sonography and two of 23 tumors (8.7%) were hypovascular. The concordance between contrast-enhanced sonography and CT or MRI findings was 100%.
Percutaneous Radiofrequency Ablation
Twenty-nine patients underwent 38 radiofrequency ablation sessions.
Twenty-one patients were treated in a single session. Seven patients were
treated in two sessions because of residual viable tumor (n = 4) or
local tumor progression (n = 3) and one patient in three sessions
because of local tumor progression. The day after radiofrequency ablation, CT
or MRI showed viable residual tumor in five of 30 tumors (16.7%).
Contrast-enhanced sonography of 22 of these 30 tumors (73.3%) showed foci of
viable tumor in four of 22 cases (18.2%). At contrast-enhanced sonography,
residual viable tumor was missed in one patient, who had a hypovascular tumor
in the posterior aspect of the left kidney. Surgical resection was scheduled,
and the patient was not included in the follow-up study. The concordance
between contrast-enhanced sono graphy and CT or MRI was 80%.
Follow-Up Imaging
The mean follow-up period was 24.6 months (range, 4–67 months). Seven
patients underwent contrast-enhanced sonography 1 year (n = 3), 2
years (n = 3), and 4 years (n = 1) after treatment because
this technique was not available at the time of percutaneous radiofrequency
ablation. Imaging showed local tumor progression in seven of 28 patients
(25.0%) after 8 months (n = 5), 2 years (n = 1), and 3 years
(n = 1). These patients were treated with radiofrequency ablation in
two sessions (n = 2), three sessions (n = 1), and two
sessions (n = 1) (Fig.
2A,
2B,
2C,
2D,
2E,
2F,
2G,
2H,
2I). Three of the five
patients who had local tumor progression after 8 months were not retreated
because of metastatic disease (n = 1) or poor general condition
(n = 2). One patient dropped out of the study after 2 years.
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To the best of our knowledge, this study was the first assessment of the performance of contrast-enhanced sonography in the long-term follow-up of renal tumors after radiofrequency ablation. The literature contains few evaluations of the effect of cryoablation of renal tumors with contrast-enhanced sonography [12, 13]. These studies were conducted with a few selected patients, and the aim was assessment of treatment efficacy [12] or the feasibility of contrast-enhanced sonography in evaluating perfusion defects at different times after cryoablation [13] rather than its performance in long-term follow-up.
Unlike CT or MRI, contrast-enhanced sonography usually best depicts renal tumors during the arterial phase. This different behavior is likely due to different contrast characteristics. Microbubble contrast agents are vascular pool agents, and iodinated and gadolinium-based contrast agents are characterized by an interstitial phase. Differentiating enhancing residual tumor from normal enhancing parenchyma can be difficult in the cases of tumors with prominent contrast enhancement during the nephrographic phase. We have found, however, that during the arterial phase, tumor generally becomes enhanced earlier than does normal parenchyma. Knowledge of enhancement characteristics of a tumor before radiofrequency ablation and review of video clips recorded during contrast administration to analyze vascular characteristics during all vascular phases is often needed to differentiate tumor from normal renal parenchyma. The enhancement characteristics of residual tumor or tumor progression reflect those observed before radiofrequency ablation.
The advantage of contrast-enhanced sonography over CT or MRI is that contrast-enhanced sonography is safe [14] for patients with impaired renal function because of the absence of urinary excretion of the contrast agent. Moreover, the technique is not contraindicated for patients with pacemakers or arthoprostheses, is less expensive than CT and MRI, and does not entail use of ionizing radiation. As reported by Clark et al. [15] the optimal frequency of follow-up imaging after radiofrequency ablation of renal tumors remains to be defined. Those authors suggested every 6 months but acknowledged that others perform imaging more frequently. We used the follow-up schedule adopted at our institution for liver metastasis and hepatocellular carcinoma.
The limitations of contrast-enhanced sonography in the evaluation of renal tumor vascularity have been described [16–18]. Mainly, the intensity of the reflected echoes significantly decreases with depth. As a consequence, deep lesions can appear to have reduced vascularity, and residual viable tumor may not be visualized. This limitation can be reduced with an imaging approach to the lesion that minimizes depth in the scanned area. It is widely overcome with the newer contrast-specific modes such as contrast pulse sequence imaging [13]. Patient-related limitations remain, as they do for all sonographic techniques. In our series, only one residual viable tumor deeply located in the left kidney in a tumor with a hypovascular pattern was missed with contrast-enhanced sonography.
There were a number of limitations to our study. It was retrospective, so the analysis of clinical and imaging records was inhomogeneous. Attenuation of the ultrasound beam, which is susceptible to patient body habitus, was an objective limit of the technique. In this series of renal tumors, percutaneous radiofrequency ablation was not preceded by biopsy. The need for biopsy was being debated at the time of the study.
Although both CT and MRI are excellent for differentiating surgical from nonsurgical renal lesions [19], both methods have low specificity in differentiating benign from malignant lesions [19–21]. No definite imaging criteria exist for discriminating carcinoma from adenoma and oncocytoma. Nevertheless, in our series the CT and MRI appearance was malignant; no fat component and no central scar were found. Percutaneous biopsy of renal masses is safe [22], and complications are uncommon. However, studies [23, 24] have shown a significant number of biopsies with nondiagnostic results, the rate ranging from 6% to 21%, and oncocytomas can be difficult to discriminate from malignant tumors that contain oncocytic cells [25].
Contrast-enhanced sonography is not a reliable tool for differentiating benign from malignant renal tumors, although visualization of a tumoral pseudocapsule can be a useful sign in the differential diagnosis [26]. The possibility exists that a benign lesion might have been ablated and followed up. We believe, however, that this possibility does not reduce significantly the strength of our findings. Our aim was to compare on the basis of enhancement characteristics of the lesion before and after ablation the perfor mance of contrast-enhanced sonography with that of CT or MRI in the assessment of results of radiofrequency ablation.
Another limitation of this study was that different models of sonographic, CT, and MRI equipment were used over the years. This limitation might have been inevitable in our clinical setting. Nevertheless, all sonographic equipment operated with highly performing contrast-specific software. If our preliminary results are confirmed in larger series, contrast-enhanced sonography is a promising technique for evaluation of patients who have undergone radiofrequency ablation. During follow-up, contrast-enhanced sonography is an effective and less expensive alternative to CT, especially for patients with marginal renal function.
In our practice, in which we have more than 5 years of experience in follow-up imaging of renal tumors managed with radiofrequency ablation, we perform contrast-enhanced sono graphy and CT or MRI every 4 months in the first year after the treatment. Afterward, contrast-enhanced sonography is performed every 4 months and CT or MRI every 8 months if findings are normal. Should contrast-enhanced sonography show hyper-enhancing foci of local tumor progression, CT or MRI is performed to confirm the findings and to address the issue of another percutaneous radiofrequency ablation treatment. In the case of false-positive findings on contrast-enhanced sonography, the initial follow-up schedule is followed. As shown by our results and those in other series [2, 27], local tumor progression is found in a minority of patients when appropriate selection criteria for radiofrequency ablation are used. As a conse quence, if CT or MRI were used for all patients with no local tumor progression at contrast-enhanced sonography, the clinical role of this technique would be minimal in practice. We strongly believe that contrast-enhanced sono graphy is useful for accurate assessment of successful management of hypervascular tumors. In our series, false-negative results were observed only in the case of hypovascular tumor. Larger series of patients are needed to confirm the results of this study.
Acknowledgments
We thank Carmine Tinelli, with the scientific head office of the Istituto
Di Ricovero e Cura a Carattere Scientifico, San Matteo Foundation, Pavia
University, Italy, for assistance with statistical analysis.
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