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Original Research |
1 Department of Radiology, University of Wisconsin, 600 Highland Ave., E3/311
CSC, Madison, WI 53792-3252.
2 Department of Surgery, Division of Urology, University of Wisconsin, Madison,
WI.
Received January 22, 2008;
accepted after revision April 30, 2008.
Address correspondence to J. L. Hinshaw.
Abstract
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MATERIALS AND METHODS. A total of 30 percutaneous renal cryoablations (mean tumor size, 2.1 cm) in 30 patients (mean age, 67.0 years) and 60 laparoscopic renal cryoablations (mean tumor size, 2.5 cm) in 46 patients (mean age, 67.4 years) were compared. The size of the tumor, procedural complications, hospital charges, length of hospital stay, and tumor follow-up parameters were recorded. Monitoring after ablation was performed every 3 months using contrast-enhanced MRI or CT.
RESULTS. Both percutaneous cryoablation and laparoscopic cryoablation of solid renal masses had a high technical success rate (30/30 [100%] and 59/60 [98.3%]). There was no significant difference in the rate of residual disease (3/30 [10%] and 4/60 [6.7%], p = 0.68), and the secondary effectiveness rate is 100% for both groups to date. One renal mass treated using laparoscopic cryoablation had a local recurrence, but none of the masses treated using percutaneous cryoablation had a recurrence. The disease-specific survival is 100% in both groups with no significant difference in the mean follow-up time (14.5 vs 14.6 months, p = 1.0) or major complication rate (0/30 [0%] vs 3/60 [5.0%], p = 0.55). For the treatment of solid renal masses, percutaneous cryoablation was associated with 40% lower hospital charges (mean, $14,175 vs $23,618, p < 0.00001) and a shorter hospital stay (mean ± SD, 1.1 ± 0.3 vs 2.4 ± 2.1 days; p < 0.0001) than laparoscopic cryoablation.
CONCLUSION. Although certain tumors require laparoscopic intervention because of the location or size of the tumor, percutaneous renal cryoablation is safe and effective and is associated with lower charges when used for the treatment of small renal tumors.
Keywords: ablation • cryoablation • kidney disease • oncologic imaging • renal cell carcinoma • renal masses
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Although long-term data are not yet available, the results of previous studies suggest that laparoscopic cryoablation and open cryoablation are both safe and effective for treating RCC when compared with other surgical therapies [4–8]. The effectiveness rate for cryoablation of renal tumors at 5-year follow-up in one laparoscopic study approached 90% [4]. Only early feasibility studies of percutaneous cryoablation of RCC have been performed to date, but data from those studies suggest that percutaneous cryoablation of RCC is both safe and effective [9–17].
In patients who are candidates for cryoablation using either the percutaneous or the laparoscopic approach, percutaneous cryoablation may have certain compelling advantages because of, first, the ability to use CT, sonography, or MRI guidance to visualize the tumor, ice ball, and surrounding structures; second, the minimal invasiveness of the percutaneous technique; and, third, the virtually painless nature of tissue freezing, which allows the procedures to be performed with the patient under moderate sedation and local anesthesia if preferred [9, 15, 16, 18–22].
The purpose of this study was to retrospectively compare the results, morbidity, and associated charges of percutaneous versus laparoscopic cryoablation for the treatment of solid renal masses.
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Patient and Tumor Characteristics
Records were reviewed for all patients who underwent percutaneous or
laparoscopic cryoablation of a solid renal mass or masses. Before 2003,
laparoscopic cryoablation and percutaneous radiofrequency ablation were the
only renal ablation methods offered at our institution. Starting in 2003 with
the advent of small-diameter percutaneous cryoprobes, percutaneous
cryoablation was offered if the renal tumor was in a posterior or
posterolateral location and the puncture path was free of overlying bowel. As
techniques were developed to allow displacement of bowel and other structures
(e.g., hydrodissection), we became more aggressive in our approach to
percutaneous cryoablation. Specifically, we now consider every patient for
percutaneous cryoablation, even those with anterior and inferior masses that
in our initial experience would have been treated with laparoscopic
techniques. However, in general, patients with anterior tumors that had no
clear percutaneous approach were offered laparoscopic cryoablation. Patients
with bowel overlying the tumor were also, in general, offered laparoscopic
ablation. Note that although tumor size is an important consideration for
determining if a patient should undergo a surgical resection or an ablative
procedure, we do not consider it to be a critical factor for determining if a
patient should undergo percutaneous or lap aroscopic ablation. All procedures
were performed with the patient under general anesthesia and an overnight
hospital stay was planned before the procedure for patients undergoing
percutaneous cryoablation.
Between October 2003 and August 2007, 35 renal masses in 35 patients were treated with percutaneous cryoablation. Between February 2001 and August 2007, 64 renal masses in 62 patients were ablated using a laparoscopic technique. Five of the percutaneous cryoablations were performed to complete treatment of residual disease identified after a previous laparoscopic or percutaneous cryoablation, and these patients were excluded from our calculations because there may be an associated bias to the clinical outcome. Note that although these ablations were considered to be a continuation of the initial ablative therapy, the results were included in the primary effectiveness rate for the associated laparoscopic procedure. Two patients who underwent lapa roscopic cryoablation had two tumors ablated at a single session, and these patients were also excluded because inclusion would bias the charges data and possibly the clinical outcomes. Thus, our study group was made up of 30 patients who underwent percutaneous ablation of 30 lesions and 60 patients who underwent laparoscopic ablation of 60 lesions (Table 1).
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Patients underwent follow-up with contrast-enhanced CT or MRI either at our facility or locally. Although there was some variability in the timing of follow-up imaging, our standard routine includes imaging 3, 9, 12, and 24 months after the procedure, and long-term follow-up is based on the imaging findings in the first 2 years. All cases and follow-up images were reevaluated by a single author for the purposes of this study.
Patients who had findings on follow-up imaging consistent with persistent tumor within the first 6 months after the procedure were classified as having residual disease. Patients who had the first evidence of abnormal enhancement in or around the ablation zone more than 6 months after ablation were classified as having recurrent disease [23]. Evidence of residual or recurrent disease was defined as nodular enhancement within or directly adjacent to the renal tumor and zone of ablation. All patients with residual or recurrent disease were considered for a second ablation procedure.
Laparoscopic Protocol
All laparoscopic cryoablation procedures were performed by one of three
radiologists specializing in abdominal imaging with more than 35 years'
combined experience in interventional procedures and extensive experience in
ablation procedures. The procedures were performed in conjunction with one of
three urologists, all of whom have 10 years or more of experience with
laparoscopic surgical techniques.
All patients were intubated and under general anesthesia for the procedure. Either a transabdominal or a retroperitoneal approach was used depending on the location of the tumor and adjacent structures such as colon. Colon was manually displaced from the region using laparoscopic ports. Laparoscopic ports were placed so that laparoscopic sonography could be appropriately positioned and used to identify the tumor and guide placement of the cryoprobes (Fig. 1A, 1B, 1C). Cryoprobes were placed percutaneously and maneuvered into the tumor using laparoscopic sonography for guidance.
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On sonography, the anterior margin of the ice ball can be monitored, but acoustic shadowing obscures the posterior border. On CT, ice balls are low attenuation and are readily visible and, unlike percutaneous or laparoscopic sonography, the entire ice ball and surrounding structures including bowel can be visualized. The number and position of cryoprobes were determined by the size and morphology of the tumor with up to three probes for the largest tumors in this series.
Two 10-minute freeze cycles with an intervening 5-minute passive thaw were performed per lesion. The size of the ice ball was followed closely on sonography, CT, or both, and the freeze time was modified to obtain a 5- to 10-mm margin. After the ice ball completely encompassed the tumor and margin, contrast-enhanced CT was performed if the patient had a creatinine level < 1.5 mg/dL. If residual tumor was identified on contrast-enhanced CT, cryoprobes were repositioned and the residual tumor was targeted for a second treatment. If the patient had a creatinine level > 1.5 mg/dL, then immed iate imaging was deferred and additional ablation sessions were initiated if there was evidence of residual disease on subsequent follow-up imaging.
Follow-Up and Data Collection
The size of the tumor, complications, hospital charges, length of hospital
stay, and tumor follow-up parameters, along with other possible confounding
variables, were recorded. The dictated report of follow-up imaging findings
was taken to represent ground truth; all studies were interpreted by
radiologists with fellowship training in abdominal imaging and extensive
experience in evaluating follow-up imaging after ablation. All of the images
were reviewed independently by a single author. If there was a discrepancy
between the dictated report and the interpretation of that author, then a
consensus was reached in consultation with a second author.
All hospital charges associated with the initial treatment and hospital stay were used to identify a global charge for the procedure and associated hospitalization. This included, but was not limited to, all professional fees associated with the procedure, charges for cryoprobes, operating room fees, technical charges related to the procedure, anesthesia-related charges, charges associated with any imaging performed, nursing and medication charges, and hospital room charges. The charges associated with a second treatment in cases of local tumor progression or incomplete ablation were not included.
The standard terminology and reporting criteria for imaging-guided tumor ablation adopted in 2005 by the International Working Group on Image-Guided Tumor Ablation were used to describe the procedure and associated outcomes, including complications [23]. Therefore, as is standard, the term "technical success" addresses whether the tumor was treated according to protocol and was covered completely, whereas the term "technique effectiveness" refers to complete ablation of macroscopic tumor as shown at imaging follow-up.
Statistical Analysis
The differences between percutaneous cryoablation and laparoscopic
cryoablation of solid renal masses in several measures were tested. For
real-value variables such as patient age and tumor size, Welch's t
tests were used; the variables except age were log-transformed before testing
to achieve normality. For binary variables such as sex and major
complications, Fisher's exact test was used. Length of hospital stay after the
procedure was also tested by Fisher's exact test. The length of stay was
either 1 or 2 days for patients who underwent percutaneous cryoablation,
whereas it ranged between 1 and 15 days for patients who underwent
laparoscopic cryoablation. To test this variable, the observations were
categorized as 1 day, 2 days, or more than 2 days and then the 3 x 2
contingency table (three cate gories for length of stay by two groups, per
cutaneous renal cryoablation and laparoscopic renal cryoablation) was tested
by Fisher's exact test. All p values were based on two-sided tests. A
p value of less than 0.05 was considered statistically
significant.
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The mean tumor size (± SD) was 2.10 ± 0.78 cm for the percutaneous cryoablation group and 2.49 ± 0.83 cm for the laparoscopic group. This represents a significant difference (p = 0.04).
Primary and Secondary Effectiveness
There was no significant difference in the rate of residual disease between
the two groups: Three patients (3/30, 10%) in the percutaneous group and four
patients (4/60, 6.7%) in the laparoscopic group had evidence of residual
disease on follow-up imaging (p = 0.68). The three patients in the
percutaneous group were subsequently treated with a second percutaneous
cryoablation; these three patients have not shown any further evidence of
local tumor progression, resulting in a primary effectiveness rate for
percutaneous cryoablation of 90% but a combined primary and secondary
effectiveness rate of 100%. The four patients with residual disease in the
laparoscopic group died from causes unrelated to renal cancer before
retreatment (n = 1), were successfully retreated with percutaneous
cryoablation (n = 2), or continue to undergo imaging follow-up
because the findings were thought to be indeterminate (n = 1).
Because two of the patients did not or have not undergone retreatment for
residual disease, these patients are not included in the calculation of
secondary effectiveness. Therefore, the primary effectiveness rate for
laparoscopic cryoablation was 93.3% and the combined primary and secondary
effectiveness rate of laparoscopic cryoablation followed by percutaneous cryo
ablation when necessary was 100% (58/58) with one patient undergoing continued
imaging follow-up.
Failure of Therapy
One patient who underwent laparoscopic cryoablation developed local
recurrence 14 months after the procedure. The recurrence was treated with an
open partial nephrectomy. Pathology results showed RCC, clear cell type
(Fuhrman grade II). Unfortunately, 10 months after the surgery, the patient
developed another local recurrence, which was treated with percutaneous
cryoablation. The patient is now 66 months out from the original laparoscopic
cryoablation and is being treated with immunotherapy for locally advanced
disease.
No recurrence has been identified in the percutaneous cryoablation group.
Survival
No patient has died of RCC in either group. However, six patients in the
laparoscopic group died of other causes, including myocardial infarction
(n = 1), lung cancer (n = 1), hepatic adenocarcinoma
(n = 1), esophageal cancer (n = 1), pancreatic cancer
(n = 1), and squamous cell cancer (n = 1). All of these
patients died more than 30 days after the procedure. Thus, the
disease-specific survival is 100% for both groups, but the overall survival is
different for the two groups (Fig.
3).
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Complications
The complication rate was low in both groups. Four of 30 patients (13%) in
the percutaneous group and four of 60 (7%) in the laparoscopic group
experienced complications of the procedure, but the difference was not
significant (p = 0.43). However, there were fewer major complications
in the percutaneous group than the laparoscopic group (0/30 [0%] vs 3/60
[5.0%], p = 0.55). Three patients in the laparoscopic group had major
procedural complications including severe respiratory distress requiring a
15-day hospital stay; intraoperative bowel injury related to trocar placement,
not cryoablation, in a patient with a history of multiple previous surgeries
(repaired laparoscopically during the ablation and not requiring further
intervention); and postoperative atrial fibrillation. No major complications
were encountered in the percutaneous renal cryoablation group.
No transfusions or reoperations for complications were required in either patient group. Four patients in the percutaneous group and one patient in the laparoscopic group had minor procedural complications including asymptomatic perinephric hematoma, asymptomatic and self-limited urine leak identified at imaging, self-limited flank paresthesia and neuralgia, and intercostal neurapraxia.
Hospital Charges
Patients who underwent percutaneous renal cryoablation had 40% lower
hospital charges ($14,175 vs $23,618, respectively) than those who underwent
laparoscopic renal cryoablation; this difference is statistically significant
(p < 0.00001).
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The reasons for the lack of standardization or comparisons among the different ablation and guidance modalities largely reflect the patchwork history of ablation in the kidney. In general, urologists have been most interested in cryoablation as a technology, perhaps because of a long history of its use in prostate cancer. The urology community was the first to apply cryoablation to kidney cancer using an open approach [42] and, more recently, a laparoscopic approach [5, 6, 8, 43, 44]. With laparoscopic cryoablation, the kidney can be directly visualized and the puncture site and any cracks in the ice ball can be filled and covered to reduce bleeding complications. Thus, cryoprobe size is relatively unimportant. There are now several centers that have performed laparoscopic cryoablation for more than 5 years with excellent results and minimal morbidity [5, 6, 8, 43, 44].
In contrast, radiologists have traditionally favored percutaneous radiofrequency ablation likely because of extensive experience with percutaneous radiofrequency ablation in the liver and more recently in bone and lung. Radiologists have been slower than urologists to embrace cryoablation for percutaneous use because of the traditionally large cryoprobe sizes (> 13-gauge), lack of an intrinsic cautery effect, and reports of ice-ball cracking that have raised concerns of postprocedural hemorrhage [45, 46]. The recent introduction of smaller-diameter cryoprobes (14- to 17-gauge) has helped overcome resistance to percutaneous cryoablation, and several single-center series that describe percutaneous cryoablation for the treatment of RCC are now available [9, 13–17, 21, 24, 25, 47].
The published experiences of these centers cumulatively show that for percutaneous cryoablation of RCC, the procedure is both safe and efficacious in the short term. Because there is also a body of work on laparoscopic cryoablation that shows similar safety and efficacy, a comparison of these procedures would help guide physicians and patients when choosing one approach over another. Our institution is somewhat unique in that we have an integrated and cooperative renal tumor ablation team consisting of three radiologists and three urologists, all of whom have long-standing experience in tumor ablation and laparoscopic and percutaneous renal procedures. All procedures are performed jointly regardless of whether the case is a laparoscopic procedure in the operating room or a percutaneous procedure in the radiology department. This team approach removes any specialty or training biases that might be seen in other similar studies in which different groups perform different types of procedures.
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The advantages of laparoscopic cryoablation over percutaneous cryoablation for the treatment of solid renal masses are primarily related to the ability to, first, displace overlying vulnerable structures (bowel) from the tumor; second, place large cryoprobes (up to 5.0 mm) in large tumors, which allows the formation of larger and colder ice balls; and, third, easily perform hemostatic maneuvers after the probe has been withdrawn and the ice ball has melted. These advantages can be significant especially for patients who have undergone prior retroperitoneal surgery, who have tumors in places inaccessible to a percutaneous approach, and who have little retroperitoneal fat.
The advantages of percutaneous cryoablation include the following: first, the less invasive nature of the procedure, which results in rapid recovery and, in our study, in fewer major complications; second, the tamponade effect of Gerota fascia, which in our experience limits the postablation hemorrhage; and, third, the exquisite visualization of the freezing process by CT and MRI that, unlike laparoscopic sonography, can show even the posterior aspect of the ice ball. This posterior "blind spot" to laparoscopic sonography is likely responsible for several of the incomplete treatments reported after laparoscopic cryoablation in this series (Fig. 4A, 4B, 4C, 4D, 4E) and other series.
This study is not a randomized comparison of laparoscopic cryoablation and percutaneous cryoablation for the treatment of solid renal masses. Laparoscopic cryoablation has been performed longer than percutaneous cryoablation; thus, our early experience and most of the patients in our series were treated laparoscopically. However, with the advent of smaller cryoprobes and the realization that the ice ball is highly visible on CT [13], we started treating small posterior tumors with percutaneous cryoablation. As our experience increased, we became more aggressive in our case selection for percutaneous cryoablation because of the minimal patient pain and rapid recovery associated with percutaneous cryoablation. In fact, clinicians at several centers have been performing percutaneous cryoablation using only local anesthetic and moderate sedation on an outpatient basis [10]. This approach would have eliminated the inpatient and anesthesia charges in our study, and the results presented in the charges analysis would have been even more skewed toward the percutaneous approach. Also, the utilization of air, CO2, saline, 5% dextrose in water, dilator balloons, and sterile water to displace vulnerable adjacent structures now allows more aggressive percutaneous treatment of tumors that until recently would have required open or laparoscopic surgery to move these structures out of the zone of ablation [48–51].
A discussion of all of the different ablative modalities is beyond the scope of this study. However, in our experience, the principal advantage of cryoablation versus heat-based modalities is the ability to precisely track the ice ball with CT, sonography, or MRI (Fig. 5). In addition, the ice ball tends to grow in a highly uniform spherical or near-spherical configuration without unpredictable shapes that may result in injury to adjacent structures. The ability to use multiple applicators to take advantage of synergistically larger and colder ice balls is also an advantage over most radiofrequency systems. With radiofrequency ablation, the ablation zone is unpredictable in size and has a relatively imprecise correlation with imaging findings [52, 53]. However, the zone of necrosis after cryoablation has been shown to have a precise relationship with the visualized ice ball, with the lethal isotherm beginning 1–2 mm inside the edge of the ice ball [54]. Thermal ablation zones created by multiple-prong radiofrequency applicators can also be irregular [55]. It is highly likely that the combination of the lack of precision in radiofrequency ablation zone monitoring and an irregular ablation zone shape is responsible for some of the renal pelvis and ureteral injuries reported in the radiofrequency literature.
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Some authors have reported less damage to urothelial structures with cold than with heat [56–58], but we think that the primary advantages of freezing are that the ice ball has a consistent growth pattern; is highly visible; and is easily monitored, ensuring complete ablation of the tumor and sparing of adjacent vulnerable structures. Despite differences in the cause of tissue destruction, both cryoablation and radiofrequency ablation have proven to be effective for treating RCC and the selection of ablation modality will likely depend on local factors, experience with the different ablation technology, and characteristics of the patient population. At our center, we favor radiofrequency ablation for the treatment of kidney tumors in patients with coagulopathy because of the theoretic decrease in associated bleeding risk or for the treatment of benign but vascular tumors such as angiomyolipomas. Cryo ablation is our treatment modality of choice for all other renal tumors eligible for ablation.
The topic of ablation versus surgery is also beyond the scope of this study, but suffice it to say that the trend in both fields is toward less invasive approaches [9, 24, 59]. Radical nephrectomies are becoming less common, and partial nephrectomies are increasingly being performed with laparoscopic techniques. This change is a result of multiple studies that have shown that the clinical outcome and technical success of laparoscopic partial nephrectomy for small renal tumors are comparable to those seen with radical nephrectomy and open partial nephrectomy [60–62]. A recent study of laparoscopic partial nephrectomy with 5-year follow-up (mean tumor size = 2.9 cm) identified a 94.6% primary effectiveness rate, a 2.7% local recurrence rate, a 100% cancer-specific survival, and a 13% complication rate [63].
Our results with both percutaneous cryoablation and laparoscopic cryoablation of solid renal masses compare very favorably. As a result, we expect this trend toward minimally invasive approaches to continue. Regardless of the advances in both surgery and ablation, it is highly unlikely that one technique will make the other obsolete, especially because ablation has intrinsic limitations for treating large tumors, tumors where the bowel cannot be displaced by percutaneous techniques, or tumors where the renal vein or inferior vena cava are involved. The need for continuing innovation in both areas highlights the need for cooperation between disciplines and a multidisciplinary approach to treating patients with renal cancer.
The lower charges for percutaneous cryoablation in this study are not surprising given the less invasive nature of most percutaneous procedures as well as the expense associated with time in the operating room. Our results are very similar to those of a prior study performed using a computer model to analyze hypothetical data compiled from a metropolitan center. That study showed the cost of laparoscopic cryoablation to be 2.3 times higher than the cost of percutaneous cryoablation when performed with the patient under conscious sedation [64]. Our study evaluated the actual (not hypothetical as in the previous study) hospital charges associated with cryoablation and identified a small but statistically significant increase in charges for the laparoscopic approach (factor of 1.7). The smaller cost savings seen in our study compared with the other study [64] is almost certainly due to the routine use of general anesthesia and the overnight stay of patients undergoing percutaneous ablation at our institution. Because some institutions perform percutaneous ablation as an outpatient procedure with the patient under moderate sedation, the cost savings would be even more dramatic in that setting. In a different study, investigators performed a cost analysis of percutaneous renal radiofrequency ablation compared with open partial nephrectomy and laparoscopic partial nephrectomy. The results of that study showed that the laparoscopic and open techniques were associated with significantly higher costs (by a factor of 1.6 and 1.7, respectively) than the percutaneous technique [65]. In the surgical literature, multiple studies have evaluated the costs associated with surgical treatment of RCC [66–69]; all have shown that laparoscopic and open surgical techniques have similar costs but are higher than the cost of percutaneous ablation reported in the current study and a prior study [46].
The primary limitations of this study are related to the study design. This is a retrospective study of a heterogeneous patient population, leading to inevitable differences between the study groups. Specifically, the tumors were significantly larger in the laparoscopic group than in the percutaneous group (mean, 2.1 vs 2.5 cm, respectively). However, because all of the previously cited studies performed with both percutaneous and laparoscopic techniques have shown excellent local control for tumors less than 3.0 cm, this difference is not likely to have had a significant effect on the technical outcomes. Also, the mean follow-up was slightly shorter in the percutaneous group than in the laparoscopic group as a result of the more recent introduction of percutaneous cryoablation. This is also associated with a possible bias related to the learning curve of performing these procedures. The initial ablations were performed using laparoscopic techniques and the expectation is that results would improve with experience. As a result, one might expect that the early results with laparoscopic techniques might be worse than the more recent results with both laparoscopic and percutaneous procedures. However, note that the results were excellent with both laparoscopic and percutaneous techniques throughout our experience, suggesting that this issue is not a significant one.
An additional limitation of the study is that we evaluated the hospital charges associated with the two procedures. The hospital charges represent a valid but indirect measure of the true cost because they do not take into account the actual reimbursement levels for the various components of the charges. Also, as indicated earlier, we believe that involvement of an anesthesiologist, the use of general anesthesia, and an overnight hospital stay for patients undergoing percutaneous cryoablation of solid renal masses who often come from far distances maximize patient comfort and safety. However, this practice varies by institution and adds significantly to the charges associated with the percutaneous technique.
The results of our study show an excellent short-term efficacy and safety profile for both percutaneous cryoablation and laparoscopic cryoablation of solid renal masses. No significant difference was found in primary or secondary effectiveness for tumor control or complications at this early stage. However, percutaneous cryoablation was associated with lower charges than laparoscopic cryoablation and was associated with a shorter hospital stay.
Based on the results of this study, percutaneous cryoablation appears to show promise for the treatment of RCC in appropriate candidates and may have advantages over laparoscopic cryoablation. Continued research is needed to evaluate the long-term outcomes of cryoablation therapy for RCC, particularly in comparison with conventional and laparoscopic surgery.
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