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1 Department of Radiological Sciences, University of Messina, Via Consolare
Valeria-Gazzi, Messina 98100, Italy.
2 Clinic of Urology, University of Messina, Messina 98100, Italy.
Received October 13, 2003;
accepted after revision December 10, 2003.
Address correspondence to G. Ascenti
(gascenti{at}unime.it).
Abstract
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SUBJECTS AND METHODS. Thirty-two patients with 40 renal masses suspicious for renal cancer (mean diameter, 3.1 cm) were prospectively studied with contrast-enhanced second-harmonic sonography during IV administration of a second-generation sonographic contrast agent. The sonographic criteria for the presence of a pseudocapsule were a peritumoral hypoanechoic halo on conventional gray-scale imaging and a rim of perilesional enhancement, increasing in the tardive phase of the examination, on contrast-enhanced second-harmonic imaging. Multiphasic helical CT or dynamic MRI or both were performed in all patients.
RESULTS. Final diagnoses of the 40 renal masses were as follows: hemorrhagic cysts, five; angiomyolipomas, four; lymphomas, four; metastasis from lung cancer, one; and renal cell carcinomas (RCCs), 26. Histologic diagnosis of RCC was surgically obtained in all patients. Nephron-sparing surgery was performed in 12 of 26 RCCs, and radical nephrectomy was performed in the remaining 14. At pathologic examination, pseudocapsule was found in 14 (53.8%) of 26 RCCs. On conventional sonography, the presence of a pseudocapsule was detected in 3 of 14 RCCs (sensitivity, 21%). Sonographic contrast-enhanced harmonic imaging revealed the presence of pseudocapsule in 12 of 14 RCCs (sensitivity, 85.7%). In the remaining 12 RCCs with either absent or extensive neoplastic infiltration of pseudocapsule seen at pathologic evaluation, pseudocapsule was not visible on either conventional or contrast-enhanced second-harmonic sonography. The pseudocapsule was not visible in any of the 14 noncancerous renal masses on either conventional or contrast-enhanced sonography.
CONCLUSION. Sonographic contrast-specific imaging with a second-generation contrast agent is effective in improving the sonographic visualization of tumoral pseudocapsule. This finding could be useful both in the sonographic diagnosis and in the choice of conservative surgery for renal cell carcinoma. The potential role of second-harmonic contrast-enhanced sonography in the management of renal cell carcinoma should be investigated in larger series and compared with the findings of state-of-the-art MRI and CT.
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Nephron-sparing surgery is the technique of choice for the management of neoplasms involving both kidneys or an anatomic or functional solitary kidney to preserve renal function. Moreover, this surgical technique has been observed to produce positive results in patients with low-grade, low-stage, peripherally located RCC [5–10].
Among the criteria that allow nephron-sparing surgery, presurgical identification of a peritumoral pseudocapsule achieves greater importance [11]. The pseudocapsule is composed of fibrous tissue and compressed renal parenchyma and is usually associated with low histologic grade RCC [12, 13].
Interest in the study of renal masses with contrast-enhanced sonography has been reawakened by the advent of sonographic second-generation contrast agents and the development of contrast-specific real-time imaging based on both microbubble harmonic response and subtraction techniques.
The purpose of this study was to assess the ability of contrast-enhanced second-harmonic sonography to detect the presence of a pseudocapsule compared with conventional gray-scale sonography. This finding could be useful both for diagnosing RCC and for planning a surgical approach to it.
To our knowledge, this is the first report on this topic in the literature.
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Renal masses were incidentally detected in 29 patients during routine abdominal sonography.
Microscopic or macroscopic hematuria or palpable abdominal masses or both were present in six patients. Renal masses were detected on CT during renal follow-up examinations in two patients with von Hippel-Lindau disease and in one patient with a history of nephrectomy for carcinoma.
Imaging Technique
All sonographic examinations were performed with an Esatune scanner
(Esaote), a dedicated second-generation contrast-agent machine equipped with
CnTI (Esaote) real-time contrast-specific software, which produces images on
the basis of both maintenance of microbubbles at low acoustic pressure and
subtractive imaging techniques. A convex or sector phased array 3.5-MHz probe
was used.
Approval of the ethics committee of our institution and informed consent were obtained.
Our study had two phases. First, conventional gray-scale sonography was performed to localize and assess the size and the echostructural characteristics of the renal lesions and the presence of pseudocapsules. Sonography with real-time contrast harmonic software was performed by switching the scanner to the contrast-specific mode by pressing a button on the console. A second-generation contrast agent (SonoVue [an aqueous suspension of stabilized sulfur fluoride microbubbles], Bracco) approved for radiologic clinical use in Europe, consisting of a stabilized aqueous suspension of sulfur hexafluoride microbubbles with a phospholipidic shell, was adopted for this study. A single or double 2.4-mL dose of contrast medium was administered through an antecubital vein, and examination of renal mass perfusion was evaluated in real time. Acoustic pressure ranged between 0.35 and 0.55 kPa to minimize breaking microbubbles.
A digital video clip of the entire examination was stored in the hard disk of the sonographic scanner. The sonographic criterion to define the presence of a pseudocapsule on conventional gray-scale imaging was the presence of a peritumoral hypoanechoic halo [14–16]. On contrast-enhanced second-harmonic imaging, a rim of perilesional enhancement, increasing in the latter phase of the examination, was considered to represent a pseudocapsule with reference to the behavior of pseudocapsule in hepatocellular carcinoma [17].
Moreover, in equivocal cases, breaking the microbubbles with high-acoustic pressure pulse was used to distinguish contrast enhancement of pseudocapsule from surrounding high-amplitude signals, such as those sent by hyperechoic renal sinus fat, which were not completely canceled by the software.
Multiphasic helical CT or dynamic MRI or both were performed in all 38 patients (CT in 26 patients, MRI in eight, and both in four patients).
Image Interpretation and Analysis
Three reviewers who had not performed any of the examinations viewed both
the conventional and the contrast-enhanced second-harmonic sonograms
separately. The reviewers were all dedicated abdominal radiologists who
routinely interpret abdominal sonograms. No clinical information was provided
to the reviewers. Dynamic images were reviewed on a sonographic unit. The
examinations were randomized, and the reviewers were not aware of the results
of the other imaging examinations and the results of the other reviewers. All
reviewers viewed the images in the same order in four separate sessions, with
an interval of 2 weeks between each session.
Statistical Analysis
The McNemar test, a nonparametric procedure, was used to compare the
sensitivity of conventional gray-scale and contrast-enhanced second-harmonic
sonography in detecting a pseudocapsule.
[18]. A p value of
0.05 was considered statistically significant.
Interreviewer agreement between each pair of reviewers in detecting pseudocapsule was assessed for each sonographic technique using kappa statistics and associated 95% confidence intervals. Kappa values of 0.01–0.20 were considered to represent minor agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, high agreement; and 0.81–1.00, almost perfect agreement, beyond chance [19].
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Final diagnoses of the 40 renal masses were as follows: hemorrhagic cysts, five; angiomyolipomas, four; lymphomas, four; metastasis from lung cancer, one; and RCC, 26.
Twenty-six patients had one lesion, four patients had two lesions (two RCCs in two patients and two hemorrhagic cysts in the remaining two), and two patients had three lesions (lymphomas in one and RCCs in one patient with von Hippel-Lindau disease).
Diagnosis of hemorrhagic cyst was obtained by MRI signal intensity of the lesions and absence of contrast enhancement on both CT and MRI. Angiomyolipoma was diagnosed when macroscopic intralesional fat was identified on CT or MRI. Lymphomas and metastases were diagnosed by percutaneous renal biopsy guided by CT or sonography.
Histologic diagnosis of RCC was surgically obtained in all patients. Nephron-sparing surgery was performed in 12 of 26 RCCs, and radical nephrectomy, in the remaining 14. At pathologic examination, pseudocapsule was found in 14 (53.8%) of 26 RCCs. On conventional sonography, the presence of a pseudocapsule was detected in three of these 14 RCCs (sensitivity, 21%).
Two reviewers detected the presence of a pseudocapsule in 12 of 14 RCCs on contrast-enhanced harmonic sonography (sensitivity, 85.7%); a third reviewer detected 11 of 14 pseudocapsules (sensitivity, 78%) (Figs. 1A, 1B, 1C, 1D, 1E, 2A, 2B, 2C, 3A, 3B and Table 1). The kappa agreement statistic regarding the presence or absence of pseudocapsule was 1.00 for reviewers 1 versus 2, 2 versus 3, and 1 versus 3 for conventional sonography, and it was 1.00 for reviewers 1 versus 2 and 0.76 for reviewers 2 versus 3 and 1 versus 3.
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Increased sensitivity of contrast-enhanced second-harmonic sonography in the detection of pseudocapsule compared with conventional sonography was statistically significant (p < 0.05).
In the remaining 12 RCCs with either absent or extensive neoplastic infiltration of the pseudocapsule seen at pathologic evaluation, a pseudocapsule was not visible either on conventional or contrast-enhanced second-harmonic sonography. The pseudocapsule was not visible in any of the 14 noncancerous renal masses either on conventional or contrast-enhanced sonography.
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The presence of a pseudocapsule is considered a useful sign for discriminating RCCs from other renal tumors. Indeed, it is almost exclusively seen in early-stage, low-grade RCC and oncocytoma. On the other hand, pseudocapsule is usually absent in metastases, hemorrhagic cysts, and angiomyolipomas [11, 12, 14, 15, 21, 22].
Parenchyma-sparing nephrectomy is the technique of choice for the treatment of neoplasms involving both kidneys or an anatomic or functional solitary kidney to preserve renal function. Moreover, in recent years, this conservative surgical procedure has gained widespread acceptance in the treatment of patients with small, low-grade, peripherally localized renal carcinomas and normal contralateral kidneys [6, 7, 9]. Diagnostic imaging for presurgical planning is crucial in the choice of either conservative or radical management. Presurgical identification of a pseudocapsule represents a significant finding in deciding whether to manage RCC with conservative surgery [11]. Partial nephrectomy or simple enucleation may be indicated when a pseudocapsule is detected [11, 12, 21].
MRI is reported as the most effective imaging tool for showing the pseudocapsule, with a sensitivity ranging between 61% and 93% [11, 12, 20, 21]. T2-weighted imaging is the most sensitive technique for detecting the pseudocapsule, which appears as a rim of hypointensity interposed between hyperintense tumor and normal renal parenchyma. [11, 12, 20].
Although several authors have reported a low sensitivity of CT in detecting pseudocapsules [12, 20, 23], a recent article has claimed that high-resolution MDCT allowed identification of a pseudocapsule with high accuracy [24]. Further studies are necessary to compare the accuracy of MDCT and contrast-enhanced second-harmonic sonography in the depiction of pseudocapsules.
The identification of a peritumoral hypoanechoic halo, which reveals the presence of a pseudocapsule, is reported as a specific sign, but with low sensitivity, on conventional gray-scale sonography [14–16]. Our study confirms this finding because tumoral pseudocapsule was visible in only three of 14 encapsulated RCCs (sensitivity, 21%).
In recent years, the development of second-harmonic contrast-specific imaging techniques and the introduction of second-generation sonographic contrast agents, such as SonoVue, have opened new possibilities for sonography in renal applications, by allowing the detection of perfusion of both macro- and microcirculation of renal parenchyma and solid masses [25]. Contrast-enhanced second-harmonic modes produce images on the basis of nonlinear effects of microbubble contrast agents, displaying the enhancement in gray scale. They also offer a unique opportunity to reduce the background signals from the surrounding structures, thereby improving microbubble detection and significantly increasing the contrast-to-tissue ratio in the image [25, 26].
SonoVue is a second-generation sonographic contrast medium composed of a stabilized aqueous suspension of sulfur hexafluoride microbubbles with phospholipidic shells. The resonance frequency of this agent is 1.5–3.0 MHz, with second harmonics between 3.0 and 6.0 MHz. The mean diameter of the bubbles is 2.5 µ m allowing both transpulmonary and transsinusoidal passage. This contrast agent has a strong harmonic response, which allows high enhancement by working with contrast-dedicated software at low acoustic pressure in real time [27]. On contrast-enhanced second-harmonic sonography, the pseudocapsule appears as a rim of peritumoral enhancement. Because a pseudocapsule is composed of fibrous tissue and compressed renal parenchyma, enhancement can occur late. Therefore, we have observed that in some cases, a pseudocapsule appears as a hypoechoic halo in the first contrast enhancement and becomes hyperechoic in the delayed-contrast phase. After the microbubbles are broken with high-acoustic pressure pulse, the pseudocapsule returns as a hypoanechoic halo.
In our series, contrast-enhanced second-harmonic sonography showed pseudocapsules in 12 of 14 RCCs (sensitivity, 85.7%). No false-positive finding was seen in the remaining 12 nonencapsulated RCCs. A distinct pseudocapsule was not detected in any angiomyolipomas, complex cysts, lymphomas, or metastases. Our data show that contrast-enhanced second-harmonic sonography, with a second-generation sonographic contrast agent, such as SonoVue, is effective in improving the sonographic visualization of a tumoral pseudocapsule, which is a useful sign both in the differential diagnosis of RCC and in the choice of a conservative surgical approach. The sensitivity of this technique may compete with that of MRI in the presurgical detection of pseudocapsules. Concerning this issue, we believe that contrast-enhanced second-harmonic sonography may be the examination of choice in patients who cannot undergo MRI for contraindications or claustrophobia. Further advantages of contrast-enhanced sonography with respect to MRI are lower cost, greater availability, and shorter examination time. Furthermore, when imaging methods are compared, a major advantage of sonography arises from the fact that most solid renal lesions are incidentally detected during abdominal sonography. Sonographic contrast imaging may be useful in increasing confidence in the diagnosis of RCC in such incidentally detected renal masses before the patient leaves the sonographic laboratory [26].
In conclusion, the promising role of second-harmonic contrast-enhanced sonography in the management of RCCs should be more closely investigated in larger series and compared with state-of-the-art MRI and CT.
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