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1
Division of Radiology, A21, The Cleveland Clinic Foundation, 9500 Euclid Ave.,
Cleveland, OH 44195.
2
Present address: Department of Radiology, Hacettepe University Hospital,
Sihhiye, Ankara, Turkey.
3
Department of Urology, Section of Minimally Invasive Surgery, The Cleveland
Clinic Foundation, Cleveland, OH 44195.
Received April 28, 1999;
accepted after revision August 16, 1999.
Presented at the annual meeting of the American Roentgen Ray Society, New
Orleans, May 1999.
Abstract
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MATERIALS AND METHODS. Twenty-one patients (men, 11; women, 10; age
range, 36-84 years; average age, 65.5 years; SD, 11.9) with 23 small renal
masses (
4 cm) underwent laparoscopic renal lesion cryoablation. Twenty
patients (22 masses) underwent followup MR imaging on the first day after
surgery, 12 (13 masses) at 1 month, 16 (18 masses) at 3 months, 14 (15 masses)
at 6 months, and 12 (12 masses) at 12 months. Three radiologists
retrospectively reviewed MR images for the signal intensity, characteristics,
and size of cryolesions. CT-guided needle biopsy was performed 6 months after
cryoablation (18 patients) and no evidence of malignancy was discovered.
RESULTS. Including all lesions at all times on T1-weighted images, cryolesion signal intensity was isointense to renal parenchyma (47/76, 61.8%) or isointense with hyper- or hypointense foci (7/76, 9.2%). On T2-weighted images, almost all lesions (72/76, 94.7%) were isointense or hypointense, and there was a hypointense rim between the cryolesion and renal parenchyma in 38.2% of lesions (29/76). A thin peripheral rim of enhancement was noted in 19.7% (14/74) of lesions. Cryolesions decreased in size an average of 61.5% (SD, 22.82; n = 12) at 1 month, 78.7% (SD, 13.5; n = 17) at 3 months, 83.5% (SD, 24.3; n = 15) at 6 months, and 94.2% (SD, 8.1; n = 11) at 1 year after cryoablation (one patient was not scanned 1 day after cryoablation and was not included in our calculations).
CONCLUSION. After renal cryoablation, MR imaging revealed common signal characteristics such as low-signal-intensity rims on T2-weighted images, enhancement patterns such as thin peripheral rims, and interval size changes.
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4 cm) unilateral
localized renal cell carcinoma. The reproducibility and reliability of renal
cryoablation have been confirmed in several animal models
[1,2,3,4,5,6,7].
Additionally, some clinical reports describe renal cryoablation in human
subjects [8,
9]. With the development of
supercooled minimally invasive cryodelivery systems and the availability of
reliable real-time sonographic monitoring, laparoscopic cryoablation is
possible for some patients
[10]. We describe the
sequential MR imaging findings from the first-day postoperative examination to
the 1-year follow-up after laparoscopic renal cryoablation. |
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4 cm) peripheral exophytic enhancing lesions located at least 1 cm from
the collecting system. Each lesion fulfilled established CT criteria for
suspected renal malignancy without evidence of metastatic disease.
Intraoperative needle biopsy (Table
1) confirmed renal cell carcinoma in 13 lesions; probable
oncocytoma in one; angiomyolipoma in one (treated for size of 4 cm); and
necrotic tissue, hemosiderin deposition, or benignancy in eight. Patients with
benignancy at biopsy underwent cryoablation based on preoperative imaging
features and the possibility of a false-negative biopsy. Two patients had two
foci of renal cell carcinoma in the same kidney.
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A liquid nitrogen-based cryounit was used (Cryomedical Sciences, Rockville, MD). Cryoablation was performed with an insulated conic-tip cryoprobe (diameter, 4.8 mm) and a 2- or 4-cm freeze zone, depending on the size of the renal tumor. With real-time sonographic guidance, the tip of the cryoprobe was advanced into the tumor and a double freeze-thaw cycle was performed. A rapid freeze was performed (tip temperature from -185°C to -195°C) until the edge of the ice ball circumferentially extended 1 cm beyond the tumor margin on sonography. After removing the cryoprobe, hemostatic pressure was maintained on the puncture site with a piece of oxidized cellulose (Surgicel; Johnson & Johnson Medical, Arlington, TX), a bioabsorbable topical hemostatic agent.
Twenty patients (22 lesions) underwent MR imaging on the first day after surgery, 12 (13 lesions) at 1 month, 16 (18 lesions) at 3 months, 14 (15 lesions) at 6 months, and 12 (12 lesions) at 12 months. MR imaging was performed on a 1.5-T scanner (Vision; Siemens, Erlangen, Germany). The MR imaging protocol included T2-weighted axial turbo spin-echo (TR range/TE, 3000-4000/99; flip angle, 80°; echo train length, 11; echo spacing, 16.5 msec; acquisitions, four) and unenhanced and contrast-enhanced (0.1 mmol/kg) ([gadolinium] Magnevist; Berlex Laboratories, Wayne, NJ) T1-weighted fast low-angle shot axial and coronal sequences (TR/TE, 142/4.4; flip angle, 80°; acquisitions, one) with a matrix of 128 x 256 and a slice thickness of 5 mm.
Three radiologists retrospectively reviewed the MR images, and decisions were made by consensus. The signal intensity of the cryolesions and perinephric changes were characterized on T1-weighted, T2-weighted, and gadolinium-enhanced images relative to the uninvolved kidney. The homogeneity and borders of the cryolesions were evaluated. The size of each lesion was measured on gadolinium-enhanced T1-weighted axial and coronal images. The volume of each lesion was estimated using the formula for the volume of a prolate ellipse (V = transverse dimension x anteroposterior dimension x craniocaudal dimension x 0.5236), and the interval volume change between each scan and the first-day scan was calculated (postoperative day—x volume — postoperative day-1 volume / postoperative day-1 volume).
In 18 patients, CT-guided core biopsies were performed at 6 months. None of the biopsies showed evidence of malignancy; however, biopsies revealed fibrosis, hemosiderin, benign renal parenchyma, and ischemic necrosis.
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Thirteen lesions in twelve patients were scanned approximately 1 month after cryoablation. Cryolesion size diminished an average of 63.3% (range, 28.7-85.0%; SD, 23.2; n = 12) from the first day after cryoablation (Table 2). On T1-weighted images, lesions were homogeneously isointense (8/13, 61.5%), and four lesions were hyperintense (4/13, 30.8%). On T2-weighted images, the lesions were isointense (4/13, 30.8%), hypointense (4/13, 30.8%), or hypo- or isointense with heterogeneity (5/13, 38.5%). None of the lesions was hyperintense to normal renal parenchyma. Nine lesions (9/13, 69.2%) showed a peripheral hypointense rim on T2-weighted images. Five lesions had partial rims (5/13, 38.5%) and four had complete rims (4/13, 30.8%). Four lesions (4/13, 30.8%) showed a thin rim of peripheral enhancement after gadolinium administration.
Eighteen lesions in 16 patients were scanned 3 months after cryoablation. Cryolesion size decreased an average of 78.7% (range, 65.4-97.7%; SD, 13.5; n = 17) from the first day after the cryoablation examination (one patient was not scanned 1 day after cryoablation and was not included in our calculations). On T1-weighted images, more lesions were hyperintense (8/18, 44.4%) than at prior intervals, but most remained isointense to renal parenchyma (10/18, 55.6%). On T2-weighted images, cryolesions were isointense (4/18, 22.2%), hypointense (5/18, 27.8%), or heterogeneously hypointense (9/18, 50%). Some lesions had a complete (4/18, 22.2%) or partial (1/18, 5.6%) hypointense rim. Nine lesions (9/18, 50%) had an enhancing rim whereas seven (7/18, 38.9%) had no enhancement after gadolinium administration (one patient with two lesions received no gadolinium).
Fifteen lesions in 14 patients were scanned 6 months after cryoablation. Cryolesion size decreased an average of 83.5% (range, 20-100%; SD, 24.3; n = 15) from the first day after the cryoablation examination. One lesion was identified as a cortical defect at the site of the previously seen cryolesion. On T1-weighted images, most lesions were isointense (10/14, 71.4%), with fewer hyperintense (3/14, 21.4%) or hypointense (1/14, 7.1%) lesions. On T2-weighted images, 57.1% (8/14) were heterogeneously hypo- or isointense. Four were isointense (4/14, 28.6%), one was hypointense (1/14, 7%), and one was hyperintense (1/14, 7%). On T2-weighted images, two lesions had partial (1/14, 7.1%) or complete (1/14, 7.1%) peripheral low-signal-intensity rims. One lesion (1/14, 7.1%) had a thin rim of enhancement.
Twelve lesions in 12 patients were scanned at 12 months after cryoablation. Cryolesion size decreased an average of 94.2% (range, 74.2-100%; SD, 8.1; n = 11) from the first day after the cryoablation examination (Fig. 3A,3B,3C,3D). Three lesions were identified as parenchymal defects at the site of prior cryolesion. On T1-weighted images, seven lesions were isodense (7/9, 77.8%), one was hypointense (1/9, 11.1%), and one was hyperintense (1/9, 11.1%) to renal parenchyma. On T2-weighted images, four lesions were hypointense (4/9, 44.4%), four were isointense (4/9, 44.4%), and one was heterogeneously hyperintense (1/9, 11.1%). On T2-weighted images, two lesions (2/9, 22.2%) had low-signal-intensity rims, and one had a thin rim of enhancement (1/9, 11.1%).
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Six cryolesions had a low-signal-intensity rim on T2-weighted images and a thin enhancing rim on contrast-enhanced images. Ten scans showed this combination of findings: one on the first day after the cryoablation examination, four at 1 month, and four at 3 months. No lesions had this combination of findings at 6 months or 1 year after cryoablation.
Perinephric changes were frequently seen on early images after cryoablation. These changes included ill-defined increased signal intensity on T2-weighted images suggesting fluid and focal low-signal-intensity on T2-weighted images representing Surgicel [11].
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4 cm) renal cell carcinomas and a normal
contralateral kidney can be treated with nephron-sparing partial nephrectomy
[12,
13]. Improved cryoprobe
technology and imaging-based realtime monitoring have enabled renal
cryoablation to emerge as a potential alternative to open nephron-sparing
surgery. Cryoablation of prostate, liver, and bone lesions is well described
and is performed at many institutions
[8]. Two clinical case reports
describe the use of cryoablation for palliation in advanced renal carcinoma,
for a large angiomyolipoma, and for a centrally located renal cell carcinoma
[8,
9]. A larger series from our
institution provides the basis for this report
[10]. To our knowledge, no MR
imaging studies describe the features of the kidney after cryoablation. The
soft-tissue contrast resolution and multiplanar imaging capability of MR
imaging may provide an effective method for detecting tumor recurrence in
renal cryolesions. Data from long-term follow-up examinations are crucial to
assess the usefulness of cryosurgery for treating renal tumors and MR imaging
for detecting tumor recurrence. The effects of renal cryoablation on the kidney have been studied extensively in canine, porcine, sheep, and rat models [1,2,3,4,5,6,7]. The acute histologic changes after cryosurgery are rapid coagulation necrosis and a sharp zone of transition with the normal kidney [1, 3,4,5,6,7]. A peripheral zone of incomplete necrosis surrounds the area of necrosis with a thickness ranging from 300 µm to 6.6 mm [1, 3, 5, 6]. This zone (known as the junctional zone or the sublethal injury zone) contains fibrotic tubules, glomeruli, hemosiderin deposition, and macrophages.
Radiologists must be aware of the peripheral sublethal zone to successfully plan cryotherapy and to prevent tumor recurrence. The temperature to ensure cancer cell destruction is between -20°C and -40°C [14, 15]. With a cryoprobe tip temperature of -195°C, the advancing outer edge of the ice ball is approximately 0°C [14]. This temperature is too warm to cause complete necrosis and normally leads to sublethal injury; therefore, it is important that the edge of the cryolesion be approximately 1 cm beyond the visible margin of the targeted tumor.
After cryotherapy, rapid coagulation necrosis is followed by the clearing of coagulated cellular debris with minimum inflammatory reaction [6]. Fibrosis of the injured area starts 14 days after the production of the cryolesion [6]. At the cellular level, a temperature of -40°C leads to cell membrane rupture and cell death caused by the formation of intracellular water crystals and intracellular protein coagulation. Vasoconstriction and thrombosis of distal arterioles and venules, occlusion of larger segmental renal artery branches, and the autoimmune destruction of previously cryoinjured tissue [4] further enhance cellular destruction.
The signal intensity on T1-weighted images was insufficient to delineate the cryolesion, especially its borders with the kidney. Including all times frames, most T1-weighted images depicted lesions that were isointense to renal parenchyma (47/76, 61.8%) or isointense with hyper- or hypointense foci (7/76, 9.2%). The borders of cryolesions were well depicted on T2-weighted images because of the relative hypointensity of the lesion compared with normal renal parenchyma. Gadolinium-enhanced images revealed the clearest border delineation during first-day postoperative and 1-month examinations. Therefore, we used these images to measure the size of the cryolesions. On T2-weighted images, a peripheral 2- to 4-mm hypointense zone along the border of the lesion and the normal kidney was helpful in delineating lesion borders (Fig. 1A,1B,1C,1D). This rim was present in 50-70% of patients up to 2 months after cryoablation, but was seen less frequently (20-25%) thereafter. The rim was not caused by chemical shift artifacts because it was seen irrespective of the frequency encoding direction. We believe the rim may represent the sublethal injury zone described in animals [1, 3, 5, 6]. The presence of such a well-defined zone with a markedly different intensity from the rest of the kidney may play an important role in recognizing marginal tumor recurrence. A similar finding was found in MR imaging studies of liver lesion cryoablation and was described as a potential indicator of cryotherapy success [15].
The signal intensities of cryolesions on T1- and T2-weighted images were somewhat variable, but there were some trends. Lesions were generally isointense on T1-weighted images (47/76, 61.8%) and iso- or hypointense on T2-weighted images (72/76, 94.7%). The origin of these signal intensities may result from the coagulation necrosis of cryotherapy, but we have no histologic confirmation in this study.
All cryolesions showed a dramatic progressive decrease in size (Fig. 3A,3B,3C,3D). None of the cryolesions remained stable or increased in size. Based on the animal models, the decrease in volume represents evolving fibrosis and scarring leading to shrinkage of the lesion [6]. Any increase in size of a cryolesion should be viewed with suspicion.
Some cryolesions had a peripheral hypervascularized rim on T1-weighted gadolinium-enhanced images (Fig. 2A,2B). This rim was seen in fewer than 10% (2/22, 9.1%) of lesions at first-day postoperative examination, but in 30-50% of lesions at 1-3 months. Thereafter, it was seen in up to 20% of lesions. In hepatic cryolesions, a complete hypervascularized rim suggests the complete cryodestruction of a lesion, whereas an incomplete rim indicates residual tumor (Altmeyer K et al., presented at the International Society for Magnetic Resonance in Medicine scientific meeting, May 1997). This finding is not as consistent in our group of patients because most cryolesions did not have an enhancing rim. However, if hypervascularized rims were present, they would have been better depicted on fat-suppressed gadolinium-enhanced T1-weighted images. On non-fat suppressed gadolinium-enhanced T1-weighted images, hypervascular rims could have been masked by adjacent high-signal-intensity perinephric fat. Most patients who underwent fat-suppressed imaging had an enhancing rim.
In our study, it was rare to view a low-signal-intensity rim on T2-weighted images and thin rim enhancement on enhanced images on the same study. Both rims suggest cryotherapy success in the liver. However, because the histologic mechanism of rims is unknown, it is difficult to speculate on why they may or may not occur together. Additionally, as cryolesion volume diminishes, rims become increasingly difficult to discern. In our study, the scarcity of rim enhancement at 6 and 12 months may be a function of small cryolesion size.
After surgery, we noted no significant perinephric change other than a small amount of either proteinaceous or hemorrhagic fluid, which appeared isointense to muscle on T1-weighted images and hyperintense to muscle on T2-weighted images. Because peripheral lesions were cryoablated, it was difficult to delineate the cryolesion from the perinephric changes in some patients, especially on the first day after the cryoablation examination.
This study has five limitations. First, fat-suppressed images may have helped better assess cryolesion enhancement characteristics. Second, our classification scheme for signal-intensity determination was subjective. Third, a significant percentage of renal lesions had negative findings on intraoperative biopsy. Because of technical difficulties guiding a percutaneously placed needle with a laparoscopic probe, our false-negative rate was likely higher than the typical false-negative rate of needle biopsy. However, in the conventional treatment of a solid renal mass, surgery is based on preoperative imaging alone, and no intraoperative biopsy is obtained before proceeding with radical nephrectomy. Fourth, some patients were not compliant with scheduled follow-up examinations or biopsy, and some patients underwent MR imaging at other institutions; these patients were excluded from our study. Fifth, preoperative MR imaging was unavailable for most patients.
In conclusion, in patients without evidence of tumor recurrence, cryolesions decrease in size over time, show peripheral rimlike enhancement, and occasionally have a low-signal-intensity rim between the cryolesion and normal renal parenchyma on T2-weighted images. On T1-weighted images, most cryolesions are isointense to the kidney, and on T2-weighted images, lesions are hypo- or isointense. Growth in cryolesion size or internal enhancement should be viewed with suspicion. Future studies with longer follow-up periods and patients with recurrent disease are needed to differentiate normal changes after cryotherapy from tumor recurrence.
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