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Imaging-Guided Radiofrequency Ablation of Solid Renal Tumors

¹ Department of Radiology, Mayo Clinic, 200 First St., Rochester, MN 55902.
² Department of Urology, Mayo Clinic, Rochester, MN 55902.

Received September 9, 2002; accepted after revision November 12, 2002.

 
Address correspondence to M. A. Farrell.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. We performed a retrospective review of imaging-guided radiofrequency ablation of solid renal tumors.

MATERIALS AND METHODS. Since May 2000, 35 tumors in 20 patients have been treated with radiofrequency ablation. The size range of treated tumors was 0.9–3.6 cm (mean, 1.7 cm). Reasons for patient referrals were a prior partial or total nephrectomy (nine patients), a comorbidity excluding nephrectomy or partial nephrectomy (10 patients), or a treatment alterative to nephron-sparing surgery (one patient who refused surgery). Tumors were classified as exophytic, intraparenchymal, or central. Sixteen patients had 31 lesions that showed serial growth on CT or MR imaging. Of these 16 patients, four patients with 10 lesions had a history of renal cell carcinoma, and two patients with 11 lesions had a history of von Hippel-Lindau disease. Four patients had incidental solid masses, two of which were biopsied and shown to represent renal cell carcinoma, and the remaining two masses were presumed malignant on the basis of imaging features. Successful ablation was regarded as any lesion showing less than 10 H of contrast enhancement on CT or no qualitative evidence of enhancement after IV gadolinium contrast-enhanced MR imaging.

RESULTS. Of the 35 tumors, 22 were exophytic and 13 were intraparenchymal. Twenty-seven of the 35 were treated percutaneously using either sonography (n = 22) or CT (n = 5). Two patients had eight tumors treated intraoperatively using sonography. Patients were followed up with contrast-enhanced CT (n = 18), MR imaging (n = 5), or both (n = 5) with a follow-up range of 1–23 months (mean, 9 months). No residual or recurrent tumor and no major side effects were seen.

CONCLUSION. Preliminary results with radiofrequency ablation of exophytic and intraparenchymal renal tumors are promising. Radiofrequency ablation is not associated with significant side effects. Further follow-up is necessary to determine the long-term efficacy of radiofrequency ablation.

Introduction

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In the past, conventional treatment for renal cell carcinoma has been radical nephrectomy [1]. Over the last two decades, nephron-sparing surgery has become an oncologically viable alternative in those patients who would be rendered anephric by a radical nephrectomy [2, 3]. Nephron-sparing surgery has been shown to be an equally effective curative treatment for patients with a single, small (< 5 cm), and clearly localized renal cell carcinoma and a normal contralateral kidney [4, 5, 6]. More recently, less invasive nephron-sparing surgical techniques have been applied to the treatment of renal cell carcinoma, including laparoscopic partial nephrectomy, radiofrequency ablation, and cryoablation [7, 8, 9]. Percutaneous approaches to nephron-sparing therapy have also been reported using radiofrequency ablation, cryotherapy, and microwave therapy in humans and transcutaneous high-intensity focused sonography in the animal model [9, 10, 11, 12, 13, 14, 15, 16]. Of the ablative methods, cryoablation is the most studied, and early results are promising. However, radiofrequency ablation is attractive as a minimally invasive treatment option in select patients, and early reports of experience with renal tumors have recently appeared in the literature. Zlotta et al. [10] reported the first radiofrequency ablation for human renal cell carcinoma in 1997. The experience with radiofrequency ablation in the treatment of renal cell carcinoma has been limited, but recent studies showing promising results have been published [17]. In a study of 19 tumors thought to have been successfully treated with radiofrequency ablation, only one had findings suggestive of residual or recurrent neoplasm: persistent focal contrast enhancement on CT at the 2-month follow-up examination [18].

This retrospective study reports our early experience with radiofrequency ablation in the treatment of human renal cell carcinoma.

Materials and Methods

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Patient Characteristics
We received institutional review board approval for a retrospective study. From May 2000 to May 2002, 35 lesions in 20 patients (15 men, five women) were treated with imaging-guided radiofrequency ablation. The patients in this study ranged in age from 27 to 80 years, with a mean age of 64 years. Patients were referred for percutaneous or intraoperative radiofrequency ablation for the following reasons: a prior total unilateral or partial nephrectomy (nine patients), a comorbidity excluding nephrectomy or partial nephrectomy (10 patients), or a treatment alternative to nephron-sparing surgery (one patient who refused surgery). All patients were referred for the procedure after a urologic evaluation.

Tumor Characteristics
Thirty-five renal tumors were included in this study; four of the tumors were in one patient with von Hippel-Lindau disease. This patient had 10 separate tumors in the right kidney that were ablated intraoperatively in one setting. Six of the patient's 10 tumors were not included in this study because the tumors could not be confidently identified on the preoperative CT scans, and no intraoperative sonograms obtained at the time of the procedure sufficiently characterized these lesions. The size range in the 35 tumors, including the treated lesions, was 0.9–3.6 cm, with a mean of 1.7 cm, as determined on the nephrographic phase of CT or MR imaging. Thirty-one lesions had a presumptive diagnosis of malignancy due to increasing size in a solid enhancing lesion on serial CT or MR imaging. Of these, 10 were in patients with a history of radical or partial nephrectomy for renal cell carcinoma, and 11 were in patients with von Hippel-Lindau disease. Four incidental solid lesions were detected on CT (n = 2), MR imaging (n = 1), or sonography (n = 1). Of these, two lesions underwent percutaneous biopsy that confirmed renal cell carcinoma. The other two remaining solid lesions each showed enhancement on CT and MR imaging. Most incidentally detected small solid renal lesions, particularly in elderly patients, would have been followed up with imaging to assess growth. However, neither patient without biopsy proof of malignancy favored this option, and a consensus decision was made by both patients and the urologist to proceed directly to radiofrequency ablation. Most solid renal lesions are carcinomas, and at our institution, biopsy of solid renal lesions has not been shown to be accurate in excluding carcinoma. A biopsy was therefore not performed in these two patients [19, 20].

Tumors were classified into three groups depending on their position relative to the renal parenchyma: exophytic, intraparenchymal, or central. For the purpose of this study, any tumor in which a component extended into the renal pelvis was classified as a central tumor. Otherwise, tumors were classified as exophytic if more than 50% of the circumference was outside the renal capsule or as intraparenchymal if less than 50% of the tumor circumference was outside the renal capsule. Tumor position was also recorded as having been in the upper, middle, or lower pole of the kidney. The kidney was divided into thirds, and the center point of the tumor was the deciding feature.

Preprocedural Evaluation
All patients were assessed with sonography before the procedure to determine whether the tumor was amenable to ablation under sonographic guidance. If the lesion was suboptimally visualized using sonography, the procedure was performed using CT guidance. An intraoperative approach was used in the setting of multiple tumors undergoing combined surgical resection and radiofrequency ablation or if there was a potential of injury to adjacent organs such as the bowel or the gallbladder.

Radiofrequency Ablation Procedure
All percutaneous procedures were performed on an outpatient basis with patients under general anesthesia. Since 1996, all radiofrequency ablations at our institution have been performed with patients under general anesthesia, although other authors have described successfully using conscious sedation for renal radiofrequency ablation [17, 18]. Two different radiofrequency ablation devices were used with techniques that have been described previously [17, 18]: the Rita (radiofrequency interstitial tissue ablation) device (Rita Medical Systems, Mountain View, CA) or the Radionics device (Radionics, Burlington, MA). With the Rita system, the Starburst needle (Rita Medical Systems) was used to treat lesions smaller than 2 cm, and the Starburst XL needle (Rita Medical Systems) was used to treat lesions larger than 2 cm.

After the target temperature was reached, the lesions were treated within a range of 12–20 min. Only one tumor was treated for longer than 15 min. The ablation was extended to 20 min in a 3.6-cm tumor because the generator was still delivering a high-output wattage at 15 min that is associated with a low-tissue impedance implying incomplete ablation. For small tumors treated with the Radionics device, the high impedance produced by desiccated tissue caused the generator to reduce the output of current after approximately 8–10 min and to remain at low power for most of the remaining 12-min cycle. Each tumor was treated with the intention of providing at least a 0.5-cm tumor-free margin, which necessitated some tumors being ablated more than once with overlapping ablation treatments. The device used depended on the preference of the radiologist.

After the ablation, the patient was observed in a radiology monitoring area for 2 hr. Immediate postoperative pain was treated with IV fentanyl or morphine, if required. The patients were then transferred to a day ward for observation. Once the patients were able to tolerate oral intake, postprocedural pain was controlled with a propoxyphene napsylate–acetaminophen combination, and patients were discharged the same day. No prophylactic antibiotics were administered.

Imaging Assessment After Ablation
All patients underwent follow-up contrast-enhanced CT or MR imaging within 48 hr of the ablation procedure. Unenhanced and contrast-enhanced arterial and nephrographic phase CT scans were obtained. If the patient's renal function prevented the administration of iodinated contrast material, contrast-enhanced MR imaging was performed instead. Continued follow-up then included either unenhanced and IV contrast-enhanced CT or MR imaging approximately 3 months after ablation and then at 6-month intervals.

Evidence of successful ablation was regarded as any lesion showing less than 10 H of contrast enhancement on CT or no qualitative evidence of enhancement after IV gadolinium contrast-enhanced MR imaging. No postprocedural biopsy was performed on any tumor.

Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
Thirty-five tumors were treated in 20 patients. There were 22 exophytic tumors, 13 intraparenchymal tumors, and no central tumors. There were 12 upper-, 13 middle-, and 10 lower-pole kidney tumors. Eleven tumors were anterior, and 24 were posterior. Fifteen patients had one tumor ablated, one had two tumors ablated, one had three tumors ablated, two had four tumors ablated, and one had seven tumors ablated. Twenty-three tumors were treated with the Radionics system, and 12 tumors were treated with the Rita system. Of those tumors treated with the Rita system, 11 were treated with the active electrodes exposed to 3 cm, and one was treated with the active electrodes exposed to 4 cm. Three of the 12 were treated with two overlapping ablations. Of the 23 tumors treated with the Radionics system, four were treated with the 2-cm active electrode tip, and the remaining 19 were treated with the 3-cm active tip electrode. All 23 tumors were treated with single ablations. Twenty-seven (77%) of the 35 tumors were treated percutaneously using imaging guidance; 22 (81%) of 27 tumors, using sonographic guidance; and five (19%) of 27 tumors, using CT guidance. Eight (23%) of the 35 tumors were treated intraoperatively using sonographic guidance in two patients. One of these patients had von Hippel-Lindau disease and was scheduled for radiofrequency ablation of four tumors using CT guidance; however, because of the close proximity of one lesion to the colon, a decision was made to expose the kidney surgically. The second patient had multiple renal cell tumors in a solitary right kidney and underwent combined surgical partial nephrectomy and sonographically guided radiofrequency ablation of four of the tumors.

The length of the follow-up ranged from 1 to 23 months (mean, 9 months; median, 9 months). Eighteen patients had contrast-enhanced CT follow-up examinations, seven had contrast-enhanced MR imaging follow-up, and five had both CT and MR imaging follow-up.

No treated tumor showed enhancement on contrast-enhanced CT or MR imaging (Figs. 1A, 1B, 1C and 2A, 2B). On CT after radiofrequency ablation, the mean ± SD enhancement in the lesion after IV contrast administration was 1.4 ± 1.5 H.

View larger version (110K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —51-year-old man with renal transplant in left lower quadrant. Transverse sonogram of transplant shows 2.4 cm hypoechoic exophytic mass (straight arrows) arising from medial aspect of kidney. Sonographically guided needle biopsy (not shown) confirmed renal cell carcinoma. Tumor was treated with radiofrequency ablation. Bladder (curved arrow) was decompressed with transurethral catheter before ablation.

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —51-year-old man with renal transplant in left lower quadrant. Fat-saturated unenhanced (B) and contrast-enhanced (C) axial T1-weighted gradient-echo MR images obtained 14 months after ablation show no enhancement in tumor (arrows).

View larger version (135K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —51-year-old man with renal transplant in left lower quadrant. Fat-saturated unenhanced (B) and contrast-enhanced (C) axial T1-weighted gradient-echo MR images obtained 14 months after ablation show no enhancement in tumor (arrows).

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —66-year-old man with history of right partial nephrectomy for renal cell carcinoma. Axial gadolinium-enhanced MR image shows 2.2-cm enhancing mass in upper pole of left kidney (arrows). This mass was treated with sonographically guided percutaneous radiofrequency ablation.

View larger version (157K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —66-year-old man with history of right partial nephrectomy for renal cell carcinoma. Axial contrast-enhanced CT scan obtained 17 months after radiofrequency ablation shows focal encapsulated nonenhancing mass (arrow) at site of previous tumor.

Three patients developed ipsilateral pain or paresthesia in the distribution of the cutaneous nerves of the lumbar plexus and flank (Figs. 3A, 3B). All three patients were treated via the psoas muscle using CT guidance. Two of the patients were treated with the Rita device, and one patient was treated with the Radionics device. The first patient experienced pain immediately after the procedure in the groin and the upper thigh that resolved spontaneously after 2 hr. The second patient developed pain and hyperesthesia in the ipsilateral flank 2 days after the procedure that persisted for 15 days. A trial of oral gabapentin was attempted at a low dose of 100 mg per day, but the patient experienced drowsiness, and the medication was stopped. The symptoms resolved spontaneously. The third patient developed severe pain with associated numbness on the lateral trunk and proximal thigh approximately 4 days after the procedure. Abdominal CT and MR imaging of the spine showed no obvious cause for the pain. The patient continues to have moderate pain and paresthesia in the lower inguinal area 9 months after the procedure. A neurology consultation concluded that the symptoms were consistent with injury to the lumbar plexus. A trial of oral gabapentin was initiated but was stopped by the patient because of drowsiness.

View larger version (165K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —72-year-old woman with history of left radical nephrectomy and right partial nephrectomy for renal cell carcinoma. Contrast-enhanced CT scan obtained with patient in decubitus position shows 1.2-cm solid mass (arrow) in medial aspect of right kidney.

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —72-year-old woman with history of left radical nephrectomy and right partial nephrectomy for renal cell carcinoma. CT scan shows CT-guided translumbar approach used to perform radiofrequency ablation of mass with patient under general anesthesia. Note electrode traversing psoas muscle and exposed tine overlaying anterior border of psoas muscle (arrow). After procedure, patient complained of groin pain and paresthesia in distribution of femoral branch of genitofemoral nerve.

One patient developed an asymptomatic postprocedural perirenal fluid collection measuring 4 cm, incidentally noted on a follow-up CT scan obtained 10 months after radiofrequency ablation. The fluid collection is currently under observation and thought to be insignificant.

Seventeen of the 18 patients who were treated percutaneously were discharged the same day. One patient was admitted over-night for personal reasons.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Radiofrequency ablation is a proven effective treatment for both primary and secondary hepatic tumors [21, 22]. Attention has recently begun to focus on radiofrequency ablation as a minimally invasive treatment option for renal cell carcinoma, and various outcomes have been reported [8, 17, 18].

Our study found that radiofrequency ablation produced an area of ablated renal tissue that showed no evidence of residual enhancing or recurrent tumor in any patient with a mean follow-up of 9 months. The success rate in our series is higher than that reported by others. Gervais et al. [17] were unsuccessful in treating two central tumors. Our success may be due to the location of the tumor within the kidney and the fact that we did not treat a central tumor. Centrally located tumors are more difficult to successfully treat as a result of heat loss caused by the large amount of vascularity in the central kidney. During radiofrequency ablation, heat loss occurs at the needle tip mainly through convection by means of blood circulation [23, 24]. Goldberg et al. [23] have shown that perfusion-mediated cooling reduces the coagulation necrosis achievable with radiofrequency ablation and that reduction of blood flow during radiofrequency application increased coagulation in human liver metastases. Perfusion-mediated cooling is particularly important adjacent to the renal hilum because of the relatively large central vessel that receives approximately 12% of the cardiac output. We did not have any central tumor in our series, which likely explains our higher success rate compared with those series that did have central tumors.

In contrast, peripheral tumors that are surrounded by less parenchyma are not in contact with large vessels and are insulated by perinephric fat, making them ideally suited to radiofrequency ablation. In the Gervais [17] study, all five exophytic tumors, including two lesions measuring 3.4 and 3.5 cm, were free of enhancement at 6 months. One of our exophytic lesions was 4 cm and was successfully treated with two overlapping ablations. Thus, it would appear that exophytic lesions are more likely than central lesions to be successfully treated. Exophytic tumors greater than 3 cm can be treated but will require overlapping or staged treatments.

Other authors have reported less overall success with radiofrequency ablation of renal tumors. Rendon et al. [8] reported 11 tumors treated with radiofrequency ablation in which pathologic examination after ablation showed a residual viable tumor volume of 5–10% in seven of the 11 tumors at the ablation margin. A few points should be raised regarding this study that may explain the authors' results. Histologic characteristics of the lesions were made after staining with H and E. However, accurate prediction of tumor viability using H and E is not reliable, and special stains are required to avoid an overestimation of residual tumor in lesions treated [25, 26]. In addition, the radiofrequency generator, the RF2000 (RadioTherapeutics, Sunnyvale, CA), used by Rendon et al. [8] in their study, supplies up to 90 W of power and has now been replaced by a more powerful 200-W RF3000 (Radio-Therapeutics) radiofrequency generator. In vivo studies have shown a correlation between power deposition and the diameter of the resultant coagulation [27]. Finally, a newer algorithm provided in the instructions for use of this radiofrequency system recommends two cycles of radiofrequency ablation per deployment of the needle electrode and that ablation should not be terminated until the current ceases to flow and power output falls to zero.

No major complications were encountered. Three patients experienced postprocedural pain in the distribution of a lumbar plexus branch. All three patients were treated with a posterior approach via the psoas muscle using CT guidance. The lumbar plexus is formed in the psoas muscle from the anterior rami of the upper four lumbar nerves. The iliohypogastric nerve, ilioinguinal nerve, lateral cutaneous nerve of the thigh, and femoral nerve emerge in that order from the lateral border of the psoas and course downward. The genitofemoral nerve emerges from the anterior border of the psoas muscle and runs along the inferior border of the muscle. These nerves are vulnerable to thermal injury if a transpsoas approach is used that involves heating the psoas muscle or its anterior surface. As a result, we now avoid heating the psoas to minimize the risk of thermal injury to these nerves. Pavlovich et al. [18] reported two patients who had increased hip pain on flexion that resolved at 48 hr and 2 weeks, respectively. Although two of our three patients reported spontaneous resolution of symptoms, one patient has persistent numbness, pain, and hyperesthesia in the ipsilateral lower inguinal area 2 months after the radiofrequency procedure.

There are some shortcomings in our retrospective study. We did not confirm histologic diagnosis of most of the ablated tumors. However, over 90% of solid renal masses are renal adenocarcinoma. Previous work at our institution has shown the inaccuracy of needle biopsy of both frozen and permanent sections of renal lesions [19, 20]. Thirty-one lesions in our study showed growth on serial imaging. Twenty-one of these enlarging lesions were in patients with either a history of renal cell carcinoma or von Hippel-Lindau disease. Extensive experience with patients who have von Hippel-Lindau disease has shown that solid renal masses on CT are due to clear cell neoplasms, thus making biopsy unnecessary [28].

Also, our criterion for success was lack of enhancement on CT or MR imaging. We did not perform a biopsy on any lesion after ablation to evaluate residual tumor. The extent of tumor necrosis after radiofrequency ablation has previously been shown to correlate closely with findings on contrast-enhanced CT and MR imaging [23, 29]. Areas devoid of contrast enhancement on CT and MR imaging after radiofrequency ablation have been shown to correspond to the histopathologic areas of coagulation to within 2 mm [25]. Gill et al. [9] performed laparoscopic cryoablation on 34 tumors that were followed up with contrast-enhanced MR imaging. Twenty-four patients who showed no enhancement on MR imaging had negative findings 3–6 months later at CT-guided biopsy of the ablated area.

Although this finding is reassuring, previous radiofrequency ablation work in the liver has shown that when the region of ablation closely approximates the original tumor size, CT can underestimate residual disease [25]. This occurred in two patients in the study by Rendon et al. [8], in which the patients were found to have residual tumor at the ablative margin, whereas on CT the area did not show any enhancement. However, all patients in our practice who undergo radiofrequency ablation have follow-up contrast-enhanced CT or MR imaging after 3 months and then every 6 months to detect any new areas of enhancement in the region of the ablated tumor or an increase in lesion size. To date, no patient in our current study has developed either of these findings. We acknowledge that small renal cell carcinomas are relatively slow-growing, and our mean follow-up of 9 months may not be long enough for recurrent tumor to be detected.

Although the initial results of our study are promising, patients should be monitored for the development of local recurrence. To be considered a realistic nephron-sparing technique, radiofrequency ablation must show success rates comparable with those reported for partial nephrectomy. Ten-year recurrence rates of 4% have been reported for nephron-sparing surgery in patients with small, solitary, low-stage renal cell carcinoma most likely due to multifocality [6]. Our early experience with radiofrequency ablation for renal tumors has shown this procedure to be successful and safe. In our practice, the most common indications for radiofrequency ablation of a renal mass is in patients who have undergone either a prior radical or partial nephrectomy or in patients with comorbidity that precludes partial or total nephrectomy. In these groups of patients, radiofrequency ablation appears to be a promising alternative. Patients who were treated with radiofrequency ablation continue to be followed up, and we plan to report their longer follow-up results in the future.

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Top Abstract Introduction Materials and Methods Results Discussion References

 

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				W. S. McDougal, N. E. Tolkoff-Rubin, M. D. Michaelson, P. R. Mueller, and K. Braaten Case 28-2006 -- A 59-Year-Old Man with Masses in Both Kidneys N. Engl. J. Med., September 14, 2006; 355(11): 1161 - 1167. [Full Text] [PDF]

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				S. Kariya, N. Tanigawa, H. Kojima, A. Komemushi, Y. Shomura, Y. Ueno, T. Shiraishi, and S. Sawada Radiofrequency Ablation Combined with CO2 Injection for Treatment of Retroperitoneal Tumor: Protecting Surrounding Organs Against Thermal Injury Am. J. Roentgenol., October 1, 2005; 185(4): 890 - 893. [Abstract] [Full Text] [PDF]

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				E. M. Merkle, S. G. Nour, and J. S. Lewin MR Imaging Follow-up after Percutaneous Radiofrequency Ablation of Renal Cell Carcinoma: Findings in 18 Patients during First 6 Months Radiology, June 1, 2005; 235(3): 1065 - 1071. [Abstract] [Full Text] [PDF]

				J. M. Lee, J. K. Han, S. H. Choi, S. H. Kim, J. Y. Lee, K. S. Shin, C. J. Han, and B. I. Choi Comparison of Renal Ablation with Monopolar Radiofrequency and Hypertonic-Saline-Augmented Bipolar Radiofrequency: In Vitro and In Vivo Experimental Studies Am. J. Roentgenol., March 1, 2005; 184(3): 897 - 905. [Abstract] [Full Text] [PDF]

				M. D. Gillett, M. T. Gettman, H. Zincke, and M. L. Blute Tissue Ablation Technologies for Localized Prostate Cancer Mayo Clin. Proc., December 1, 2004; 79(12): 1547 - 1555. [Abstract] [PDF]

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