Retroperitoneal laparoscopic cryoablation of small renal tumors: intermediate results
Article Outline
Abstract
Objectives
To present our experience with laparoscopic renal cryoablation with up to 3 years of follow-up. Laparoscopic renal cryoablation remains a viable option for the treatment of small peripheral renal masses in patients with significant comorbidities. Although partial nephrectomy has been shown to be a safe and reliable method of renal parenchymal preservation, laparoscopic cryoablation still requires longer term data to prove its efficacy.
Methods
Twenty patients with small renal masses (1.4 to 4.5 cm) underwent laparoscopic renal cryosurgery at our institution. A retroperitoneal laparoscopic approach was used to expose the kidney. Intraoperative ultrasound guidance was used to localize the lesions and monitor iceball formation. A double-freeze technique was used. Needle biopsies of solid masses were performed intraoperatively.
Results
Renal biopsies revealed renal cell carcinoma in 11 of the 20 patients. Of these 11 patients, none had evidence of recurrent disease at last follow-up, and follow-up scans showed no enhancement of any lesions. Of the 8 patients with follow-up of 2 years or greater, 4 had complete resolution of the renal lesions. The remainder had lesions that were reduced and stable in size. Complications included surgical re-exploration to evaluate pancreatic injury in 1 patient and failure to ablate a lesion in another.
Conclusions
Laparoscopic renal cryoablation appears to be an effective tool for ablation of small renal lesions. A moderate length of follow-up continues to demonstrate efficacy because no patients had growth of treated pathologic lesions or developed metastasis to date. Continued maturation of data is necessary to determine the long-term efficacy.
Increasingly, nephron-sparing approaches are used for small renal lesions (4 cm or less). The complications of open partial nephrectomy have been acceptably low, and the local recurrence rate has been 5% to 7%.1, 2 Preservation of renal parenchyma in a solitary kidney obviates or delays the morbidity and mortality of dialysis and also may be beneficial for patients with two kidneys. Minimally invasive approaches now include laparoscopic partial nephrectomy and laparoscopic renal cryoablation.3
Cryoablation is a technique using small probes and circulating liquid nitrogen or argon gas to freeze and ablate tissue. Its recent resurgence has been in part because of improved cryosurgery units that rapidly cool to target treatment temperatures and high-resolution ultrasonography that precisely target lesions and accurately monitors the freezing process. Cryosurgery for prostate4, 5 and liver6, 7 disease is currently used at many medical centers. Early reports of renal cryosurgery in animal models8, 9 and in humans3, 10, 11, 12, 13 have been encouraging.
To our knowledge, fewer than 50 cases of laparoscopic cryoablation of renal tumors3, 10 have been reported. We report our experience with this procedure performed on 20 patients with intermediate follow-up of as long as 3 years.
Material and methods
Patients
Between October 1997 and January 2001, 20 patients underwent laparoscopic renal cryoablation (Table I). In all patients, preoperative computed tomography (CT) or magnetic resonance imaging (MRI) showed a solid or complex renal mass less than 4 cm in size. Patient age ranged from 40 to 84 years. Metastatic disease was not evident on any staging studies, including laboratory tests, chest radiography, CT, and/or MRI. All patients were thoroughly counseled regarding the procedures that were standard of care, including radical nephrectomy and partial nephrectomy and that cryoablation has no long-term follow-up with large numbers of patients. Patients with central renal lesions were not considered for treatment by this technique.
TABLE I. Preoperative patient characteristics
| Pt. No. | Sex | Age (yr) | Preoperative Imaging | Size (cm) | Side | Location |
|---|---|---|---|---|---|---|
| 1 | F | 81 | Solid | 2.5 | L | Lower pole |
| 2 | F | 81 | Solid | 2.5 | R | Lower pole |
| 3 | F | 43 | AML | 2.3 | R | Upper pole |
| 4 | F | 62 | Complex cyst | 2.6 | L | Lower pole |
| 5 | M | 76 | Solid | 1.4 | L | Midpole |
| 6 | M | 72 | Solid | 2.1 | L | Upper pole |
| 7 | M | 43 | Solid | 3.4 | R | Lower pole |
| 8 | M | 54 | Solid | 1.4 | L | Upper pole |
| 9 | F | 52 | Complex cyst | 2.7 | R | Upper pole |
| 10 | F | 71 | Solid | 2 | R | Lower pole |
| 11 | M | 75 | Solid | 2.5 | L | Midpole |
| 12 | M | 55 | Complex cyst | 2.5 | L | Lower pole |
| 13 | M | 79 | Solid | 3.1 | R | Upper pole |
| 14 | M | 71 | Solid | 1.6 | L | Midpole |
| 15 | F | 65 | Solid | 2.2 | L | Midpole |
| 16 | F | 54 | Solid | 2.4 | R | Upper pole |
| 17 | M | 75 | Solid | 4 | R | Midpole |
| 18 | F | 82 | Solid | 2.6 | L | Midpole |
| 19 | M | 82 | Solid | 3.4 | L | Lower pole |
| 20 | M | 84 | Solid | 4.5 | R | Midpole |
Technique
A retroperitoneal approach was used for all cases, regardless of the position of the tumor. The patient was placed in a lateral decubitus position after the induction of general anesthesia. A Foley catheter and orogastric tube were placed. A 2-cm incision was made at the tip of the 12th rib and the retroperitoneum entered. A balloon dilator (Origin Medical, Menlo Park, Calif) was inflated to 1 L to create a working space. A balloon-tipped Hasson trocar (Origin Medical) was then placed and carbon dioxide insufflated to 15 mm Hg. Two additional 5-mm working trocars were placed (Fig. 1).
FIGURE 1.
Port placement for right retroperitoneal laparoscopic cryoablation. Patient’s head is to the left. Note, central balloon port with 5-mm ports to either side.
The kidney was dissected free of Gerota’s fascia and widely exposed. Renal ultrasonography with a 10-mm laparoscopic side-firing articulating transducer (Toshiba Medical Systems, Tustin, Calif) was used to localize the lesion (Fig. 2). Our technique varied depending on whether the renal lesion was visible laparoscopically. If visible laparoscopically (eg, an exophytic lesion), biopsies were obtained with an 18-gauge spring-loaded biopsy needle and confirmed by ultrasonography to be in the renal lesion. Next, a 4.8-mm cryoprobe (CMS, Rockville, Md) was placed in the center of the lesion and confirmed by ultrasonography. If the renal lesion was not visible laparoscopically, the Hasson trocar was removed, and a transrectal ultrasound probe with needle guide was placed through this trocar site. Biopsies were then easily obtained and a needle placed in the center of the lesion. The needle was exchanged for a J-wire that was then exchanged for a 5-mm dilator and sheath placed through the Hasson trocar. A 4.8-mm cryoprobe was placed by way of the sheath and the sheath pulled back.
FIGURE 2.
Laparoscopic ultrasound probe. Note, articulating tip that allows imaging of any area of the kidney.
Freezing was monitored with ultrasonography until the iceball encompassed the lesion by at least a 5-mm margin (Fig. 3). The probe was warmed and thawing of the lesion confirmed by ultrasonography (the typical “halo” effect of thawing was usually seen). After a second freezing cycle, Avitene was placed in the former probe site using a 5-mm cannula (Davol, Cranston, RI) for hemostasis. The argon beam coagulator was available for additional hemostasis if necessary. A Jackson-Pratt drain was left through one of the port sites.
FIGURE 3.
Laparoscopic view of cryoprobe inserted into exophytic tumor during freezing. Monitoring of iceball accomplished visually and by ultrasonography.
Postoperatively, the laboratory test results were checked and the drain was removed before discharge. Patients were started on diets immediately and encouraged to ambulate. CT was performed on postoperative day 1. Postoperative imaging with MRI or CT was obtained at approximately 3-month intervals.
Results
Surgery
The results are summarized in Table II. All the procedures were accomplished laparoscopically by a retroperitoneal approach. Biopsies confirmed renal cell carcinoma in 11 patients, benign tubules in 3 patients, chronic pyelonephritis in 2 patients, oncocytoma in 1 patient, fibrosis in 1 patient, and were not done in 2 patients. All lesions were treated regardless of the biopsy result because all had been identified radiographically. The standard of care has been to treat all such renal masses without biopsy. The operative time averaged 305.9 minutes. Blood loss averaged 92.5 mL (range 50 to 200).
TABLE II. Perioperative data from retroperitoneal laparoscopic cryoablation
| Pt. No. | Biopsy Findings | OR Time (min) | EBL (mL) | Discharge Postoperative Day | Creatinine | |
|---|---|---|---|---|---|---|
| Preoperatively | Postoperatively | |||||
| 1 | RCC | 690 | 150 | 4 | 1.2 | 1.1 |
| 2 | RCC | 396 | 200 | 2 | 1 | 1 |
| 3 | None | 232 | 50 | 2 | 0.9 | 0.8 |
| 4 | No tumor | 180 | 50 | 1 | 1.0 | 1.0 |
| 5 | Chronic pyelonephritis | 240 | 100 | 2 | 0.8 | 0.8 |
| 6 | None | 260 | 50 | 3 | 1.1 | 1.1 |
| 7 | Oncocytoma | 310 | 50 | 2 | 1.2 | 1 |
| 8 | RCC | 715 | 200 | 2 | 0.9 | 0.8 |
| 9 | RCC | 490 | 50 | 2 | 0.8 | 0.6 |
| 10 | RCC | 360 | 50 | 2 | 0.7 | 0.7 |
| 11 | Chronic pyelonephritis | 430 | 150 | 2 | 1.4 | 1.3 |
| 12 | Cyst | 190 | 50 | 2 | 0.8 | 1.1 |
| 13 | RCC | 220 | 100 | 2 | 1 | 0.9 |
| 14 | Fibrosis | 300 | 50 | 9 | 1.1 | 1.0 |
| 15 | RCC | 160 | 50 | 3 | 1.1 | 1.0 |
| 16 | RCC | 235 | 50 | 3 | 0.7 | 0.6 |
| 17 | RCC | 200 | 100 | 2 | 1.2 | 1.2 |
| 18 | Benign tubules | 155 | 50 | 2 | 1.6 | 1.5 |
| 19 | RCC | 155 | 150 | 7 | 1.2 | 1.2 |
| 20 | RCC | 200 | 150 | 3 | 1.6 | 1.8 |
Postoperative course
The patients’ diets were advanced rapidly in all but 1 patient who is discussed later. Minimal analgesic agents were required. The serum creatinine remained stable. Most patients had transient rises in serum creatine kinase, lactate dehydrogenase, and aspartate aminotransferase. Patients were discharged home within an average of 2.6 days. All patients returned to regular activity by 3 weeks after surgery.
Complications
Minor complications included 5 of 11 patients with a left-sided tumor who had elevated amylase and lipase levels for 24 to 48 hours postoperatively. Another patient had electrocardiogram changes in the recovery room, but myocardial infarction was ruled out, and he did well. One patient had atrial fibrillation postoperatively, and because of this and a low hemoglobin (11.6 g/dL preoperatively and 9.2 g/dL postoperatively) was transfused 1 U of autologous blood. No urinary fistulas or significant hemorrhage occurred postoperatively.
One significant intraoperative complication occurred. One patient with a left renal lesion had a pancreatic injury. The lesion was not visible laparoscopically, and initial freezing showed suboptimal iceball formation. Troubleshooting revealed that although not apparent on ultrasonography, the cryoprobe had been advanced through and beyond the lesion. The renal lesion was then treated with standard cryoablation. Postoperatively, the patient developed abdominal pain and guarding and elevated serum amylase and lipase. CT revealed a cryoinjury to the pancreas, in addition to the well-treated renal lesion. Abdominal exploration was performed, bowel injury was ruled out, and drains were placed near the pancreas. He subsequently did well and was discharged on postoperative day 9.
Follow-up
The lesions were monitored postoperatively by serial imaging every 3 to 6 months by CT or MRI (Table III). Most of the lesions regressed com-pletely. In 1 patient, the renal lesion was apparently not ablated. The lesion remained unchanged on follow-up studies but a scar developed directly beneath the lesion. The exophytic renal lesion was 2 cm in size, located on the anteromedial aspect of the left upper pole kidney. A review of the intraoperative ultrasound scans revealed that a solid lesion had been ablated. However, because the ablation was not done under direct vision in this case, it is presumed that this “ultrasound lesion” was either artifact or inflammatory and was located directly beneath the true mass. Biopsies of the “ultrasound” lesion revealed inflammatory cells. The exophytic lesion has remained stable on serial imaging.
TABLE III. Follow-up of patients after retroperitoneal laparoscopic cryoablation
| Pt. No. | Size (cm) | Postoperative CT Finding | Latest Imaging Finding | Follow-up (mo) |
|---|---|---|---|---|
| 1 | 2.5 | No enhancement | No mass | 40 |
| 2 | 2.5 | No enhancement | No mass | 40 |
| 3 | 2.3 | No enhancement | Small scar (CT) | 35 |
| 4 | 2.6 | No enhancement | No mass (US) | 31 |
| 5 | 1.4 | Lesion not frozen | Stable size | 30 |
| 6 | 2.1 | No enhancement | 2-cm mass, no enhancement (CT) | 29 |
| 7 | 3.4 | No enhancement | 3-cm mass (MRI) | 28 |
| 8 | 1.4 | No enhancement | No follow-up | 27 |
| 9 | 2.7 | 2.1-cm mass, some enhancement | No mass (MRI) | 26 |
| 10 | 2 | 2.3-cm mass, some enhancement | No mass (MRI) | 24 |
| 11 | 2.5 | No enhancement | No follow-up | 20 |
| 12 | 2.5 | No enhancement | 2.5-cm mass, no enhancement (CT) | 17 |
| 13 | 3.1 | No enhancement | No mass (CT) | 16 |
| 14 | 1.6 | No enhancement | No mass (CT) | 12 |
| 15 | 2.2 | No enhancement | NA | 8 |
| 16 | 2.4 | No enhancement | NA | 3 |
| 17 | 4 | No enhancement | No mass (CT) | 13 |
| 18 | 2.6 | No enhancement | NA | 3 |
| 19 | 3.4 | Intralesion hemorrhage | NA | 2 |
| 20 | 4.5 | No enhancement | NA | 1 |
In cases in which the lesion was smaller and still visible, no lesion enhancement or growth has been observed. Also, the loss of normal renal tissue was minimal. The mean follow-up time was 14.2 months. In that time, no signs of recurrence of the lesions have been seen by examination, imaging, laboratory studies, or chest radiograph. In particular, no trocar site or renal fossa recurrences have developed. One lesion identified by biopsy as an angiomyolipoma took nearly 2 years to completely resolve.
Comment
Although concerns of potential urethral and rectal damage limit the extent of freezing in prostate cryosurgery, peripheral renal lesions may be frozen completely with a margin of normal renal tissue, with little risk of complications in the remainder of the normal kidney. It is unknown whether central renal lesions can be treated successfully because of the heat sink of large renal vessels and the potential for urinary fistula and obstruction if the renal pelvis is frozen.14 Recent animal studies have suggested that the renal pelvis may be frozen with little risk of fistula formation.15
Cryosurgery has been shown to ablate renal tissue successfully in several animal models. Chosy et al.15 examined renal cryosurgery in a swine model. Complete necrosis correlated with temperatures of less than −19.4°C. Areas frozen to 0.0°C to −19.4°C demonstrated necrosis in 80% of cases. Nakada et al.17, 18 performed a follow-up study in swine. They used a laparoscopic approach and a double-freeze technique and also looked at tissue necrosis. They reported complete necrosis within the iceball. Campbell et al.18 studied renal cryosurgery in a dog model. They found that the −20.0°C isotherm was at most 3.1 mm behind the edge of the iceball. No advantage was found for arterial occlusion during freezing. They also found complete tissue necrosis in the ablated area. In vivo rabbit studies with implanted VX-2 renal tumors have shown cryosurgery to be as effective as nephrectomy in control of local and metastatic disease.19
Bishoff et al.20 reported on the acute and long-term effects of cryoablation in the porcine model. Kidneys were harvested at various points ranging from 24 hours to 13 weeks after cryoablation. A single 15-minute freeze or two 5-minute freezes were performed. At 1 week, central necrosis surrounded by inflammation, hemorrhage, and fibrosis was noted. By 13 weeks, the necrotic tissue was replaced with fibrosis. Edmunds et al.21 published the results on 2 patients who underwent open cryoablation with a single 15-minute freeze followed by partial nephrectomy. Histologically, coagulative necrosis and hemorrhage were noted beyond the boundaries of the lesions.
Clinical series have reported excellent success. Chen et al.22 reported the largest experience from the Cleveland Clinic. Laparoscopic cryoablation of 35 patients has been reported. All procedures were completed laparoscopically in a mean operative time of 2.9 hours. Twenty-four of the 35 specimens demonstrated renal cell carcinoma. Patients were followed with serial MRI studies, and of the 17 patients followed up for more than 1 year, 5 had complete resolution of the lesions. Interestingly, 21 patients underwent 3 or 6-month postoperative CT-guided biopsy of the lesions. All biopsies were negative for malignancy. No recurrence in any patient was noted. Rodriguez et al.10 reported the next largest published series. Seven patients underwent cryoablation, of which three were laparoscopic. Biopsies revealed renal cell carcinoma in five of the patients. With a mean follow-up of 14.2 months, no patient had growth of any treated lesion or evidence of metastatic disease.
In our small series with intermediate follow-up, small renal lesions seemed to be successfully ablated by cryosurgery. The morbidity of laparoscopic renal cryosurgery was extremely low. This is notable because nearly 50% of our patients were older than 75 years. Bleeding was not significant, and cracking of the iceball, which has been seen in liver cryosurgery, was not seen in our series. Other than transient laboratory changes, no specifically cryosurgery-related morbidity occurred. No urinary fistulas developed, and only one injury to an adjacent structure (pancreas) occurred. Follow-up MRI showed no enhancement of the lesions and a decreased size. With the limited experience already published, a lack of postoperative enhancement of the treated lesion seems to be the most widely regarded criterion for success. Other criteria such as stability in size also can be encouraging, because growth of a treated lesion would likely lead to nephrectomy. Our series also demonstrates that apparent resolution of a radiographic mass can be seen in select cases.
Some technical concerns are worth reviewing. We used a retroperitoneal approach, which we suspect has a slightly lower morbidity than a transperitoneal approach. However, medial and upper pole lesions may be more easily accessed by a transperitoneal approach, as is advocated by Gill et al.3 Also, the “paddle” type laparoscopic ultrasound probe that is available to us yields images that are difficult to correlate with hand placement of needles into the lesion. An end-fire laparoscopic ultrasound probe with a needle guide, similar to transrectal ultrasound probes, we believe would make targeting much easier.23 Currently, direct visualization of the lesion seems to be the safest approach for accurate targeting and ablation. However, real-time three-dimensional imaging, such as MRI, would make some lesions treatable percutaneously, because ultrasound monitoring would be inadequate to visualize the entire iceball transcutaneously. Some groups are getting early experience with MRI-guided percutaneous renal cryosurgery.24 For lesions that are close to adjacent organs, such as the pancreas, spleen, or bowel, laparoscopy has the advantage of surgically separating these organs and preventing incidental cryoinjury.
The operative time quoted was quite long at 5 hours. The time required has come down to 3 hours during the past 6 cases. Most of the difference in the early experience was due to the long freeze-thaw cycle required with the liquid nitrogen systems and the learning curve inherent in laparoscopic ultrasound localization.
Conclusions
Treatment of small renal tumors by a laparoscopic approach and cryosurgical ablation is possible with low morbidity. The loss of functioning renal parenchyma appears to be minimal. Intermediate-term follow-up with MRI showed successful destruction and involution of the lesions. Long-term follow-up of a larger number of patients will be critical to determine the efficacy as measured by local recurrence, metastatic control, and survival.
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