Retrospective Comparison of Laparoscopic Partial Nephrectomy Versus Laparoscopic Renal Cryoablation for Small (<3.5 cm) Cortical Renal Masses

Abstract

Objective:

We compared perioperative and short-term outcomes of renal laparoscopic partial nephrectomy (LPN) and laparoscopic cryoablation (LCA) in patients with small (<3.5 cm) renal cortical neoplasms.

Methods:

A retrospective analysis from our prospectively established database was performed. We identified 92 patients with 95 lesions treated with LPN and 75 patients with 91 lesions treated with LCA.

Results:

The LPN and LCA groups were comparable in mean tumor size and preoperative and postoperative creatinine level (P=.495, P=.953, and P=.101) respectively. Patients undergoing LPN were younger in age (58.8 versus 69.2 years, P<.001), had a higher mean estimated blood loss (168.4 versus 66 mL, P=.005), and had a prolonged mean operative time (151.6 versus 128.6 minutes, P=.01). Six complications occurred in the LCA group and 11 in the LPN group. The median follow-up time was 21.8 months for LPN and 14 months for LCA (P<.001). Two recurrences were detected in the LCA group, and 1 recurrence was reported after LPN.

Conclusions:

In the treatment of small renal cortical neoplasms with short-term follow-up, LPN and LCA seem to be equally effective. LCA offers decreased blood loss, shorter operative time, and less morbidity. Longer follow-up is required to establish oncologic efficacy.

Introduction

Small renal cortical masses (<3.5 cm) are most commonly being diagnosed incidentally on routine cross-sectional imaging.¹ The slow-growing nature of these tumors coupled with an expanding aging population and the widespread use of advanced medical imaging, has increased the number of renal cortical neoplasms (RCNs) discovered over the last 20 years.^2,3 The majority of these masses (70%–80%) are proven to be renal cell carcinomas (RCCs), and extirpative surgery has been the standard of care in the form of open radical or partial nephrectomy. However, the surgical management of renal tumors has changed a great deal with the evolution of minimally invasive surgery and an improved understanding of the biology of these neoplasms. More than 15 years since the introduction of laparoscopic partial nephrectomy (LPN), the procedure has produced comparable results with open surgery in terms of safety and long-term oncologic efficacy and is now presently considered an accepted standard of care for patients with T1 tumors.^4–6

Because most of the patients diagnosed with small renal masses are in the sixth or seventh decade of their life, it seems natural that they often present with multiple comorbidities, making them unsuitable for major extirpative surgery. The evolution of probe-ablative procedures offers an alternative nephron-sparing and minimally invasive approach for this particular group of patients. Renal cryoablation has been the most well studied and clinically tested of the various ablative procedures and is currently practiced successfully in many academic medical centers. Cryoablation is most often performed either via laparoscopic (laparoscopic cryoablation [LCA]) or percutaneous access. Despite the lack of histologic confirmation of complete tumor resection, clinical studies published to date on cryoablation of RCNs have reported comparable oncologic control with parenchymal preservation and diminished morbidity when compared with established procedures like open partial nephrectomy.^5–7

Previous studies from our institution and other high-volume centers have reported that renal cryoablation in tumors greater than 3.5 cm in diameter has resulted in higher complication rates.^8–10 As such, we have limited the use of LCA in tumors smaller than 3.5 cm and report only on this patient population. Herein, we report our retrospective comparison in the management of small RCNs (<3.5 cm), comparing perioperative and short-term outcomes of LPN and LCA.

Subjects and Methods

A retrospective analysis from our prospectively maintained, Internal Review Board–approved minimally invasive cancer database was performed. Our study included a chart review of all patients who underwent LPN or LCA for RCNs ≤3.5 cm. Preoperative, operative, and follow-up data were evaluated. Between June 2005 and December 2008, we identified a total of 167 patients with 186 RCNs who were treated with either LPN or LCA. More specifically, 92 patients with 95 lesions underwent LPN, and 75 patients with 91 lesions underwent LCA. All procedures were performed by a single surgeon (J.L.).

The selection criteria for performing one procedure over the other were not established through a standardized protocol. Instead, a consensus was reached between the treating surgeon and each patient after a detailed discussion, during which all surgical (open and laparoscopic radical nephrectomy/LPN and LCA) and nonsurgical options (active surveillance) were considered. Significant individual factors for the final decision were age, presence of comorbidities, tumor location, previous abdominal operations, and willingness of the patient to undergo major extirpative surgery. The transperitoneal or retroperitoneal approach for both LPN and LCA was decided by the surgeon after consideration of the patient and tumor characteristics. A preoperative contrast-enhanced axial imaging study (computed tomography or magnetic resonance imaging) was performed to evaluate the location and size of the tumor and exclude the possibility of metastatic disease. For the purposes of this study, exophytic lesions were defined as ≥50% of the mass extending beyond the renal contour on axial imaging, mesophytic lesions were defined as <50% but >20% beyond the renal contour, and endophytic lesions were defined as <20% to entirely contained within the renal contour. If the mass juxtaposed the main renal artery or vein, it was considered to be hilar in nature. Intraoperatively, tumor localization and targeting were accomplished in all cases with the assistance of a flexible laparoscopic ultrasound probe (BK Medical Systems Inc., Peabody, MA).

Surgical techniques

LPN

After access to the hilum was gained, the renal vessels were identified and dissected accordingly. The tumor was adequately exposed, the kidney was mobilized, and 12.5 g of intravenous mannitol was administered prior to clamping of the renal artery with two bulldog clamps (Aesculap, B. Braun Medical, Bethlehem, PA). The tumor was excised precisely with cold scissors in warm ischemia. The base of the tumor bed, large vessels, and collecting system were sutured with interrupted figure-of-eight Vicryl^® (Ethicon, Johnson & Johnson, Somerville, NJ) sutures tied with Lapra-Ty^® (Ethicon) clips. In addition, a wet monopolar radiofrequency device (Tissue Link Floating Ball, Tissue Link Medical, Dover, NH) was used to place energy on the cortical aspects of the defect. The repair was filled with a thrombin/gelatin matrix product (FloSeal^®, Baxter Healthcare, Fremont, CA), and an absorbable bolster was placed, using horizontal mattress sutures, anchored on both ends with a Lapra-Ty, in order to close the defect nicely.

LCA

After extensive laparoscopic renal mobilization, under the guidance of a laparoscopic ultrasound probe, one to three 1.47-mm cryoprobes (Galil Medical, Plymouth Meeting, PA) were precisely deployed in order to perform a double freeze cycle followed by an active thaw cycle. Freezing was not timed, but rather was continued until the iceball was noted to extend approximately 1 cm from the tumor margin. For the hilar RCNs, where the margin was closer to the renal vasculature, an effort was made to dissect the vessels away from the tumor. The iceball was allowed to make contact with the renal artery or vein. In cases where the 1-cm margin could not be achieved, the renal artery or a segmental branch of the renal artery was clamped prior to freezing to optimize the ablation. After the second freeze cycle a short active thaw was used to remove the probes, and the iceball was then left to thaw passively. The renal surface was inspected under low insufflation pressure, and excellent hemostasis was achieved with the use of Surgicel^® (Johnson & Johnson, Irvine, CA) and the application of a thrombin/gelatin matrix product (FloSeal). Biopsies were taken for all masses. Typically three biopsy specimens were taken; however, some patients had four biopsies under another Internal Review Board–approved protocol.

Follow-up evaluations were performed at 3-, 6-, and 12-month intervals for all patients diagnosed with RCC and annually thereafter. Each evaluation included a standard abdominal imaging (computed tomography or magnetic resonance imaging), chest X-ray, and blood work (complete blood count, liver, and renal function tests). For patients in the LCA group complete tumor ablation was defined as a complete lack of enhancement of the ablated area. The operating surgeon and dedicated urologic radiologist evaluated all postoperative films.

SPSS^® (Chicago, IL) version 17 software was used for statistical analysis. Categorical and continuous data were evaluated by chi-square and Student's t tests, respectively. A P value of <.05 was considered statistically significant.

Results

From June 2005 to December 2008, in total, 167 patients with RCN were treated with either LPN or LCA in our department. The cohort included 92 patients with 95 lesions who underwent LPN and 75 patients with 91 lesions who underwent LCA. The mean age of our sample was 58.8 years (range, 37–85 years) for LPN and 69.2 years (range, 19–84 years) (P<.001) for LCA. The two groups were comparable in mean tumor size (LPN 1.9 cm versus LCA 2.0 cm, P=.495), preoperative hematocrit (40.9% versus 40.8%, P=.065), and serum creatinine levels (0.9 versus 1.1 mg/dL, P=.953). Tumor characteristics were similar for the two groups. A solitary kidney was diagnosed in 9 (12%) patients of the LCA group and in 4 (4.3%) patients of the LPN group, respectively (P<.024). Patients' demographic, preoperative, and tumor data are summarized in Table 1.

Table 1.

Demographic, Preoperative, and Tumor Data

Variable	LCA (n=75, 91 lesions)	LPN (n=92, 95 lesions)	P value
Mean age (years, range)	69.2 (19–84)	58.8 (37–85)	<.001
Sex [M/F (%)]	47/28 (62.7/37.3)	56/36 (60.8/39.2)	.883
Race [n (%)]			.253
White	56 (74.7)	78 (84.9)
African-American	6 (8.0)	4 (4.3)
Hispanic	6 (8.0)	5 (5.4)
Other	7 (9.3)	5 (5.4)
Mean ASA score (range)	1.9 (1–3)	N/A
Mean tumor size (cm) (range)	2.0 (0.4–7.5)	1.9 (0.3–4.5)	.495
Preoperative hematocrit (%)	40.8	40.9	.065
Preoperative serum creatinine (mg/dL)	1.1	0.9	.953
Location (%)			.521
Upper pole	16 (17.6)	35 (36.8)
Interpolar	31 (34.1)	19 (20.0)
Lower pole	43 (47.2)	34 (35.8)
Undescribed	1 (1.1)	7 (7.4)
Side [left/right (%)]	55/36 (60.4/39.6)	49/46 (51.6/48.4)	.862
Type of lesion [n (%)]			.962
Solid	54 (59.3)	51 (53.7)
Cystic	12 (13.2)	26 (26.3)
Solid/cystic	8 (8.8)	16 (16.8)
N/A	17 (18.7)	2 (3.2)
Depth [n (%)]			.722
Exophytic	42 (46.1)	48 (50.5)
Mesophytic	26 (28.6)	23 (24.2)
Endophytic	16 (17.6)	15 (15.8)
Hilar	5 (5.5)	5 (5.3)
N/A	2 (2.2)	4 (4.2)
Patients with solitary kidney [n (%)]	9 (12%)	4 (4.3%)	.024

ASA, American Society of Anesthesiologists; LCA, laparoscopic cryoablation; LPN, laparoscopic partial nephrectomy; N/A, not available.

The transperitoneal approach was used in 69.5% and 68.1% of LPN and LCA cases, respectively (P=.638). Patients undergoing LPN were characterized by longer mean operative time (151.6 minutes versus 128.6 minutes, P=.01) and greater mean estimated blood loss (168.4 mL versus 66 mL, P=.005) compared with LCA. The mean warm ischemia time was 24.5 minutes (range, 11–40 minutes) for LPN, and the mean cryoablation time was 6.4 minutes (range, 1–10 minutes) for the first and 5.6 minutes (range, 1–12 minutes) for the second freezing cycles, respectively. Both groups were comparable in postoperative serum creatinine (1.0 versus 1.2 mg/dL, P=.101) and hematocrit (35.9% versus 37.2%, P=.061) levels. Four (4.3%) LPN cases overall were converted to radical or open LPN in the LPN group. More specifically, in three complex cases the surgeon elected to proceed to laparoscopic radical nephrectomy because of positive margins or the tumor's proximity to the surgical margin, in frozen section; in these three cases, the central and challenging nature of the tumor was predicted, and the patients were all prepared for the radical procedure. Only 1 case was converted to open partial nephrectomy because of significant intraoperative bleeding. In the LCA group one (1.3%) conversion to LPN was recorded, because of bleeding following the thawing process. No LCA cases were converted to open surgery or to radical nephrectomy. The mean hospital stay was comparable for the two groups (2.0 days versus 1.6 days, P=.096).

The final histopathology examination revealed RCC in 69.4% of lesions excised in the LPN group (evaluation of excised tumor specimen) and 56% of lesions biopsied in the LCA group (core needle biopsy evaluation) (P=.004) (Table 2). Nine (9.9%) cases had no definitive pathology diagnosis in the LCA group, whereas positive surgical margins were identified in 2 (2.1%) patients on the final pathology report in the LPN group.

Table 2.

Intraoperative and Postoperative Data

Variable	LCA (n=75, 91 lesions)	LPN (n=92, 95 lesions)	P value
Approach [n (%)]			<.001
Transperitoneal	62 (68.1)	66 (69.5)
Retroperitoneal	23 (25.3)	15 (15.8)
N/A	6 (6.6)	14 (14.7)
Mean freeze time per cycle (minutes) (range)	6.4/5.6 (1–10)	N/A
Mean warm ischemia time (minutes) (range)	N/A	24.5 (11–40)
Mean OR time (minutes)	128.6	151.6	.01
Mean EBL (mL)	66	168.4	.005
Length of hospital stay (days)	1.6	2.0	.096
Postoperative hematocrit (%)	37.2	35.9	.061
Postoperative serum creatinine (mg/dL)	1.2	1.0	.101
Pathology [n (%)]			.004
Malignant	51 (56.0%)	66 (69.4%)
Conventional (clear cell)	33 (36.3%)	40 (42.1%)
Papillary	16 (17.6%)	15 (15.8%)
Chromophobe	2 (2.2%)	11 (11.6%)
Benign	31 (34.1%)	29 (30.6%)
Oncocytoma	17 (18.7 %)	7 (7.4%)
AML	3 (3.3%)	12 (12.6%)
Cysts/adipose-fibrous tissue	11 (12.0%)	10 (10.5%)
Unidentified	9 (9.9%)	—
Complications [n (%)]	6 (8.0%)Hemorrhage (3)Renal colic (1)Hematoma (1)Ileus (1)	11 (11.9%)Hemorrhage (5)Ileus (2)Renal hematoma (1)Pneumonia (1)Pneumothorax (1)Atelectasia (1)	<.001
Recurrences [n (%)]	2 (2.6%)	1 (1.1%)	.588
Median follow-up (months, range)	14 (1–34)	21.8 (1–48)	<.001

AML, angiomyolipoma; EBL, estimated blood loss; OR, operating room.

The complication rates for the LPN and LCA groups were 11.9% and 8%, respectively (P<.001). The LPN group had 11 (11.9%) complications, of which 3 (27.3%) were Clavien level I, 7 (63.6%) Clavien level II, and 1 Clavien level III. The complications were as follows: 5 (5.4%) renal hemorrhages requiring transfusion (2 intraoperative and 3 postoperative), 2 (2.2%) postoperative ileus cases treated conservatively, 1 (1.1%) self-contained perirenal hematoma, 1 (1.1%) case of pneumonia, 1 (1.1%) atelectasia with pleural effusion treated with drainage, and 1 (1.1%) pneumothorax treated with insertion of a chest tube. In one of the three postoperative hemorrhages, angioembolization was required to prevent the development of hematoma, whereas the other two were managed conservatively. The LCA group had 6 (8%) overall complications, of which 2 (25%) were Clavien level I, 3 (37.5%) Clavien level II, and 1 (12.5%) Clavien level III. The complications were as follows: 3 (3.1%) renal hemorrhages requiring transfusion, 1 (1.1%) renal colic treated with stent insertion on postoperative day 5, 1 (1.1%) case of transient postoperative ileus, and 1 (1.1%) perirenal hematoma that caused hydronephrosis, which resolved after endoscopic placement of an indwelling stent. No mortality was reported in the LPN group, whereas one (1.1%) patient died of non-malignant causes in the LCA group. This particular patient had a medical history of coronary artery disease with a myocardial infarction and unfortunately suffered a cardiac arrest on postoperative day 6.

The median follow-up time was 21.8 (range, 1–48) and 14 (range, 1–34) months for LPN and LCA, respectively (P<.001). For the LPN group, 85 of 92 patients (92.4%) had at least 12 months of follow-up including repeat cross-sectional imaging, and 70 of 92 (76%) had at least 18 months of follow-up including repeat axial imaging. For the LCA group, 71 of 75 patients (94.7%) had at least 12 months of follow-up including repeat cross-sectional imaging, and 66 of 75 (88%) had at least 18 months of follow-up including repeat axial imaging. Only 1 (1.1%) recurrence was recorded in the LPN group. The patient presented with a hilar recurrence with extension to the renal vein 30 months after partial nephrectomy and subsequently underwent an open radical nephrectomy. The pathology report was that of clear cell RCC. Six months after the procedure the patient shows no evidence of the disease. There were 2 (2.6%) recurrences in the LCA group. The first patient presented with a recurrence 4 months after the procedure. He was treated with an uncomplicated open partial nephrectomy, and the pathology report revealed clear cell RCC. No evidence of the disease was identified at 31 months of follow-up after partial nephrectomy. The second patient showed a local enhancement on abdominal computed tomography scan at 18 months. The patient was lost to follow-up, and no further information is available.

Discussion

The surgical decision-making for the treatment of small (<3.5 cm) RCNs has changed dramatically over the last two decades. Nephron-sparing techniques such as open partial nephrectomy or LPN currently produce results in terms of tumor control comparable to radical nephrectomy. However, in 2009, the American Urological Association released guidelines outlining the roles of various treatment options for the small renal mass.¹¹ In the guidelines, the standard treatment for masses <4 cm in the healthy patient is either partial nephrectomy or alternatively radical nephrectomy. The use of thermal ablation in this population was considered an option that should be discussed and only performed in the well-informed patient. In the unhealthy patient, both partial nephrectomy and radical nephrectomy are standards of care; however, thermal ablation is elevated to the status of a recommendation that should be considered in this population. The guidelines panel cited concerns about higher recurrence and retreatment rates associated with thermal ablation compared with tumor excision and for this reason maintained that extirpative therapy remain the gold standard of treatment for the small renal mass. Ultimately, the goal of therapy for the small renal mass, whether by partial nephrectomy or thermal ablation, is to adequately treat the lesion while preserving nephrons. Thompson et al.¹² recently reported that nephron-sparing procedures for RCNs have more favorable long-term survival compared with radical nephrectomy. Minimally invasive surgical modalities are associated with decreased morbidity when compared with open partial nephrectomy.¹³ The progress made in laparoscopic technology and the increase in technical proficiency among surgeons have made LPN the procedure of choice for the treatment of small renal masses in many centers.^6,14 The emergence of ablation techniques (most notably of LCA) has further expanded the minimally invasive treatment options available for patients with RCNs. Initially recommended only for patients with solitary kidneys or impaired renal function or to elderly patients with high surgical risk, renal cryoablation has now become a reasonable approach for all patients presenting with a small RCN (≤3.5 cm). The aim of this study was to present our experience with both LPN and LCA.

Comparing the mean age between the two groups we noted that patients undergoing LPN were considerably younger than those in the LCA group (58.8 years versus 69.2 years, P<.001). This finding is similar to that described in other series.^10,15 This is likely due to a selection bias with younger patients more commonly chosen for extirpation. In addition, the longer follow-up experience available for LPN makes it a more suitable procedure for patients with longer life expectancy.

In our LCA series we had a significantly lower mean estimated blood loss (66 mL versus 168.4 mL, P<.005) and shorter mean operative time (128.6 versus 151.6 minutes, P<.001) compared with the LPN group. Desai et al.¹⁰ similarly reported mean intraoperative blood loss of 100.8 mL for LCA and 211.3 mL for LPN (P<.001). The aforementioned findings further underline the more invasive and far more technically challenging nature of LPN, requiring substantial laparoscopic experience in order to achieve optimal results. However, the duration of hospital stay, preoperative/postoperative hematocrit, and renal functional outcomes were comparable between the two groups.

In our series, a statistically significant difference was found between the two procedures with a lower rate found in the LCA cohort (P<.001). The overall complication rate for the LCA group was 8%, which is comparable to that of other series that reported rates ranging from 10% to 14%.^16,17 Hemorrhage from the ablation site following probe removal was the most common complication (4%). Severe bleeding due to fracture of the renal parenchyma is reported to occur in between 0% and 8.1% of cases.^17–20 The relatively low incidence of renal hemorrhage seems to be in direct correlation with the size of the tumor. Lehman et al.⁸ compared results of LCA in patients with tumors <3 cm versus those with tumors >3 cm; a significant difference was observed in the complication rate for patients with larger tumors (62%) compared with smaller ones. The most frequent complication was hemorrhage requiring transfusion in 38%. The LPN group in our series had an 11.9% complication rate, which is consistent with complication rates in other published series (9%–33%).^21–23 The most common complication encountered was renal hemorrhage, which occurred in 5 (5.4%) patients. Two (2.1%) hemorrhages occurred intraoperatively: The first one was managed with transfusion and the use of hemostatic agents, whereas the second one forced the surgeon to convert the case to an open partial nephrectomy. Ramani et al.²⁴ reported an overall intraoperative bleeding rate of 3.5% out of a series of 200 patients who had LPN, whereas Abukora et al.²⁵ reported rates of 1.3% for severe and 2.6% for minor intraoperative hemorrhages.

RCC was diagnosed in 69.4% and 56% of LPN and LCA series, respectively (P<.004). This is an anticipated finding and should be attributed to sampling biopsy error as we compared the entire excised tumor specimen of the LPN group with the biopsy specimens taken during LCA. In 9 (9.9%) patients of the LCA series no definitive diagnosis was available, whereas positive surgical margins were identified in 2 (2.1%) patients in the LPN group. Our positive margin rate is consistent with the data published in other large series that reported an average rate of 3.5%.^26–28 It is worth mentioning that we prefer to perform intraoperative frozen-section biopsies in LPN cases where there is doubt about the surgical margin and for centrally located or hilar tumors.

In our study, patients were followed up for a median period of 21.8 and 14 months for the LPN and LCA groups, respectively (P<.001). Overall data from our series demonstrate fewer procedure-related complications for the LCA cohort and comparable short-term outcomes in terms of oncologic efficacy. One (1%) recurrence was recorded in the LPN group and 2 (2.6%) in the LCA group (P=.588). Several studies have managed to establish the oncologic efficacy of LCA. Gill et al.¹⁸ reported on 56 patients with 3 years of follow-up with a 75% reduction in the size of the cryolesion, while the 3-year cancer-specific survival was 98%. Hegarty et al.²⁹ reported on 66 patients who had over 5 years of follow-up; 3 patients (6%) developed tumor recurrence and required nephrectomy, the 5-year overall survival was 81%, and the cancer-specific survival was 98%. The current data require larger data sets and longer follow-up to validate the oncologic efficacy of LCA.

There are several limitations to the current study. Despite being a prospectively established dataset, there were no prospective criteria that were established to select between extirpation and ablation. Most tumors can be approached by either method; however, severely endophytic tumors can be difficult to excise laparoscopically and often must be approached with an open technique. However, cryoablation can adequately treat these lesions with precise probe placement.

Additionally, there was no significant difference in postoperative renal function between the LCA and LPN groups (1.2 ng/dL and 1.0 ng/dL, respectively, P=.101). However, this must be interpreted with caution as the majority of patients in the cohort did not have a solitary kidney. Therefore it is impossible to draw firm conclusions on the change in renal function based on the type of procedure performed.

Lastly, we report only short-term follow-up in both groups. While long-term follow-up remains critical in the evaluation of this different technique, 3- and 5-year data on cryoablation are already available and support the application of renal cryoablation in this setting.

Conclusions

The perioperative and short-term outcomes of LPN and LCA provide further evidence that LPN and LCA are equally effective for the treatment of small (<3.5 cm) RCNs. LCA has the advantage of diminished morbidity and less blood loss.

Footnotes

Disclosure Statement

No competing financial interests exist.

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