Laparoscopic Partial Nephrectomy Versus Laparoscopic Ablative Therapy: A Comparison of Surgical and Functional Outcomes in a Matched Control Study

Abstract

Background and Purpose:

Patients who are undergoing laparoscopic ablative therapy (LAT) are often older with more comorbidities in comparison with patients who are undergoing laparoscopic partial nephrectomy (LPN). A matched control study was performed to compare the surgical and functional outcomes of LPN and LAT.

Patients and Methods:

A prospectively maintained database of 250 patients who underwent nephron-sparing surgery was explored. Fifty-one LAT patients (21 and 30 laparoscopic radiofrequency and cryoablation, respectively) were matched with 51 LPN patients. A comparison of preoperative, operative, and postoperative outcomes was performed.

Results:

The groups were similar in age, sex, body mass index, preoperative estimated glomerular filtration rate (eGFR), number of comorbidities and tumor size. Patients who were undergoing LAT had a lower incidence of endophytic tumor and higher incidence of upper pole and midpolar tumors. Hilar vessels clamping was performed in LPN (47/51 patients). Mean estimated blood loss and operative time were higher in those undergoing LPN (P<0.01). There was no significant difference in transfusion rate and hospital stay, however. Mean follow-up was 27 and 18 months in LAT and LPN, respectively (P<0.01). The mean percent decline of eGFR at the last follow-up was 10 (95% confidence interval [CI]: 4–15) and 7.5 (95% CI: 4–11), respectively (P<0.43). In comparison with baseline, eGFR declined significantly (P<0. 01), but there was no difference between the groups.

Conclusion:

Despite renal ischemia, longer operative time, and higher blood loss associated with LPN, the hospital stay and long-term functional outcomes are similar to those of LAT in a matched control study.

Introduction

T he treatment of patients with small renal masses (SRMs) has changed over the past decade. There has been a departure from radical nephrectomy because multiple studies have shown that it imparts an increased risk of chronic renal insufficiency, higher rates of cardiovascular disease, hospitalizations, and mortality.^1
–3 This shift in treatment has been dramatic and has included the introduction of active surveillance for elderly and high-risk surgical candidates.⁴ The role surgery plays in the management of SRMs will persist and continue to evolve, however, because the malignant potential for SRMs cannot be determined easily.⁵

According to recent American Urological Association guidelines, partial nephrectomy (PN) has replaced radical nephrectomy as the reference standard for the management of clinical T_1a renal masses because of the importance of preservation of renal function.⁶ Nephron-sparing surgery using ablative techniques for the management of SRMs is an alternate treatment modality. Laparoscopic ablative therapy (LAT) has been associated with a low level of morbidity.^7,8 Because these techniques are also thought to be technically less difficult, they are being used in lieu of PN for high-risk and elderly patients.⁹

Both PN and ablative techniques have been shown to preserve renal function.^9,10 It has been suggested, however, that ablation may have better preservation of renal function compared with PN.¹¹ In a study by Lucas and associates,¹² the functional outcomes of radical nephrectomy, radiofrequency ablation (RFA) and PN were compared. Using multivariate analysis, the authors showed that compared with RFA, the development of stage three kidney disease was 34 and 10 times greater for radical and PN, respectively.

Direct comparisons between laparoscopic ablative treatments and laparoscopic partial nephrectomy (LPN) have been limited. The population undergoing LPN is often younger and healthier than those undergoing LAT. This increases the difficulty of directly comparing the outcomes of these two procedures. Desai and colleagues¹³ compared their experience with laparoscopic cryoablation with LPN. LPN was found to have a higher incidence of delayed complications despite a younger and healthier cohort when compared with the laparoscopic cryoablation group.

Only one direct comparison of LPN with laparoscopic RFA has been performed by Bird and coworkers,¹⁴ demonstrating similar perioperative complication rates without significant change in postoperative renal function. Using an unmatched cohort comparison, however, it is difficult to draw conclusions because treatment groups differed significantly by age, preoperative creatinine clearance, comorbidity, American Society of Anesthesiologists score, and body mass index (BMI).

The goal of this study was to evaluate the surgical and functional outcomes of LPN vs LAT within a matched control study.

Patients and Methods

After Institutional Review Board approval, a review of our prospectively maintained database was completed for LPN and LAT performed between November 2002 and December 2008. In total, 250 patients who underwent nephron-sparing surgery were evaluated. All surgeries were performed by three surgeons who regularly perform laparoscopic procedures. Of these patients, 51 received LAT: 21 laparoscopic RFA and 30 laparoscopic cryoablation. These patients were then matched by preoperative estimated glomerular filtration rate (eGFR), comorbidities, and tumor size to 51 patients who underwent LPN. Pairwise matching was performed individually between the groups. The bigger LPN group was used as controls.

Various confounding factors were matched, starting with age, baseline renal function, and tumor size and followed by comorbidities and BMI. Comorbidities were categorized into three groups: Hypertension, diabetes, and cardiovascular disease (CVD). The category of CVD consisted of patients with a history of coronary artery disease, myocardial infarction, peripheral vascular disease, cerebral vascular accident, or transient ischemic attacks. Patients were further classified based on current recommendations for staging chronic kidney disease (CKD) using their preoperative eGFR.¹⁵ Age, sex, BMI, single kidney, incidental tumor, smoking history, tumor location and depth were also evaluated.

Perioperative data including estimated blood loss (EBL), change in hematocrit (Hct), total operative time, approach, complications, change in eGFR, pathology, length of stay, and length of follow-up were analyzed. Complications were categorized as intraoperative or postoperative.

Statistical analysis

The Cockcroft and Gault equation was used to determine eGFR. All variables were analyzed using the STATA 10.1 statistical analysis software. Analysis of categorical variables was performed using chi-square or Fisher exact tests where appropriate. Analysis of continuous variables was performed using a paired t test. A P value of 0.05 or less was considered statistically significant.

Technique

The choice of surgical modality and approach was based on surgeon and patient preference as well as tumor characteristics. Our technique for performing LPN has been previously reported.¹⁶ Hilar vessel clamping was only performed with LPN.

LAT was performed via a transperitoneal (30 patients) or retroperitonal approach (21 patients). After tumor exposure, a laparoscopic ultrasound probe was used to confirm tumor location and delineate the extent and depth of the tumor. Biopsy was obtained in all patients, and this was followed by ablation. Tumors treated using laparoscopic cryoablation underwent at least two cycles of 10-minute freezing with active thaw. The cycling time for those undergoing laparoscopic RFA was typically between 5 and 10 minutes. The number of probes used for all LAT varied according to tumor size, location, and surgeon preference.

A closed drain system and Foley catheter were placed in all patients postoperatively. Blood for routine labs was drawn on postoperative days 0 and 1. For all patients, follow-up consisted of clinical examinations, regular checks of serum creatinine level, as well as abdominal imaging via either CT or MRI. The interval of clinical examination and imaging was based on tumor pathology and surgeon preference.

Results

Patient and tumor characteristics

A summary of patient demographics from both groups can be seen in Table 1. The two groups were similar in age, number and type of comorbidity, BMI, sex, as well as the number with single kidney, incidentally found tumor, and smoking history. Preoperative eGFR was also similar between groups: 87.0 mL/min LPN vs 88.0 mL/min LAT (P=0.89). The surgical procedures were also performed over a similar period.

Table 1.

Comparison of Preoperative Characteristics

	LPN	LAT	P value
Number of patients	51	51
No. women (%)	25 (49.0)	25 (49.0)	1
Mean age at Dx (range)	66.0 y (23–83)	65.7 y (27–75)	0.89
BMI (range)	29.1 kg/m² (18.2–24)	30.0 kg/m² (12.1–56.9)	0.5
No. diabetes (%)	12 (23.5)	12 (23.5)	1
No. CVD (%)	9 (17.66)	14 (27.5)	0.24
No. hypertension (%)	27 (52.9)	31 (60.8)	0.42
No. multiple comorbidities (%)	12 (23.5)	19 (37.3)	0.31
No. single kidney (%)	3 (5.9)	5 (9.8)	0.46
No. smoker (%)	18 (35.3)	11 (21.6)	0.12
No. incidental mass (%)	16 (31.4)	15 (29.4)	0.83
Mean preop eGFR (range)	87.0 mL/min (22.1–146.31)	88.0 mL/min (13.6–253.3)	0.89
No. patients in CKD stage			0.84
1 (eGFR>90 mL/min)	21	23
2 (eGFR 90–60 mL/min)	23	18
3 (eGFR 60–30 mL/min)	6	7
4 (eGFR 30–15 mL/min)	1	2
5 (eGFR<5 mL/min)	0	1

LPN=laparoscopic partial nephrectomy; LAT=laparoscopic ablative therapy; Dx=diagnosis; BMI=body mass index; CVD=cardiovascular disease; preop=preoperative; eGFR=estimated glomerular filtration rate; CKD=chronic kidney disease.

Tumor characteristics are provided in Table 2. The mean tumor size was similar between groups: 2.27 cm LPN vs 2.35 cm LAT (P=0.67) as well as the number with a central location. The only significant differences between the groups were in tumor depth (P=0.04) and location (P=0.02). Those receiving LAT had a lower incidence of endophytic tumors and a higher incidence of upper pole and midpolar tumors.

Table 2.

Comparison of Mass Characteristics

	LPN	LAT	P value
Mean mass size (range)	2.27 cm (0.80–5.10)	2.35 cm (0.99–4.90)	0.66
No. right side (%)	24 (47.1)	26 (53.0)	0.55
No. hilar (%)	4 (7.8)	2 (4.0)	0.41
No. central (%)	10 (19.6)	8 (15.7)	0.4
Tumor depth			0.04
No. endophytic (%)	6 (11.8)	0 (0)
No. mesophytic (%)	6 (11.8)	6 (11.8)
No. exophytic (%)	39 (76.5)	45 (88.2)
Tumor location			0.02
No. upper pole (%)	15 (29.4)	20 (39.2)
No. midpolar (%)	12 (23.5)	20 (39.2)
No. lower pole (%)	24 (47.1)	11 (21.6)

LPN=laparoscopic partial nephrectomy; LAT=laparoscopic ablative therapy.

Perioperative outcomes

Average operative time was 200 minutes for LPN compared with 149 minutes for LAT (P<0.001). As previously mentioned, hilar vessel clamping was performed only in the LPN group. This occurred in 47/51 patients with an average warm ischemia time of 29.3 minutes (range 13–55 min). Mean EBL was higher for patients who were undergoing LPN (141 mL), compared with LAT (54 mL) (P<0.001). The percent change in preoperative Hct to postoperative Hct, however, was similar between the two groups (P=0.74). The transfusion rates between the groups was also similar (P=0.57).

The average hospital stay was similar between groups: 1.7 days for LPN vs 1.6 days for LAT (P=0.46). Follow-up time was shorter for LPN (18 mos) compared with LAT (27 mos) (P<0.01). The perioperative data are summarized in Table 3.

Table 3.

Perioperative Data

	LPN	LAT	P value
Mean operative time (range)	200.7 min (52.8–327.0)	149.2 min (56.1–292.0)	<0.01
Mean EBL (range)	141.0 mL (10–600)	54.2 mL (0–300)	<0.01
Mean change in Hct preop to nadir (range)	6.50% (-2.9–28.4)	6.15% (-2.1–23.1)	0.74
No. received transfusion (%)	4 (8.7)	5 (9.8)	0.57
No. converted to open (%)	4 (7.8)	0 (0.0)	0.12
No. intraoperative complication (%)	4 (7.8)	1 (2.0)	0.18
No. of postop complications (%)	6 (9.8)	11 (21.6)	0.3
No. of malignant tumors on biopsy (%)	41 (80.3)	26 (50.9)	<0.01
Mean hospital stay (range)	1.7 d (1–5)	1.67 d (0–12)	0.46
Mean follow-up (range)	18.3 mos (13.0–26.8)	27.9 mos (0.4–40.0)	<0.01
Mean eGFR at 12 months (ange)	82.5 mL/min (19.2–130.8)	80.0 mL/min (11.4–210.5)	0.97

LPN=laparoscopic partial nephrectomy; LAT=laparoscopic ablative therapy; EBL=estimated blood loss; Hct=hematocrit; preop=preoperative; postop=postoperative; eGFR=estimated glomerular filtration rate.

A summary of the histologic findings can be found in Table 4. A significant difference was seen between groups for benign and malignant tumors (P<0.01). The finding of normal renal tissue was seen only in the ablative group (n=7) (P<0.01).

Table 4.

Histologic Features of Treated Renal Mass

	LAT	LPN	P value
Benign tumor			<0.01
Oncocytoma	11	4
Angiomyolipoma	4	3
Other	3	3
Malignant tumor			<0.01
Clear cell	11	31
Chromophobe	2	3
Papillary	10	6
Other	3	1
Normal renal tissue	7	0	<0.01

LAT=laparoscopic ablative therapy; LPN=laparoscopic partial nephrectomy.

Renal function changes

Renal function declined in both groups from preoperative to postoperative day 1: 87.0 to 78.9 mL/min (P<0.01) and 88.0 to 85.4 mL/min (P<0.01) in LPN and LAT, respectively. This decline in baseline renal function persisted and was still significant at 12 months follow-up in both groups: 87.0 to 82.5 mL/min (P<0.01) and 88.0 to 80.7 mL/min (P<0.01) in LPN and LAT respectively. These data are summarized in Table 5.

Table 5.

Comparison of Renal Function, Baseline to 12 Months Follow–Up

	Preoperative	Postoperative day 1	12-month follow -up	% change eGFR at 12 months	P value
Mean eGFR in mL/min all LPN (95% CI)	87.0 (78.6–95.5)	78.9 (71.9–86.0)	82.5 (74.8–90.2)	5.17%	<0.01
Preop CKD 1	117.9 (110.6–125.07)	100.5 (92.9–108.2)	106.7 (98.2–115.2)	9.49%	<0.01
Preop CKD 2	72.3 (68.9–75.8)	67.0 (52.0–72.0)	72.0 (66.3–77.8)	0.40%	0.44
Preop CKD 3 to 5	45.4 (32.8–58.0)	44.1 (29.8–58.5)	44.1 (30.8–57.5)	2.86%	0.47^a
Mean eGFR in mL/min all LAT (95% CI)	88.0 (77.0–98.9)	85.4 (73.5–97.3)	80.7 (71.0–90.4)	8.29%	<0.01
Preop CKD 1	116.2 (104.5–127.9)	107.6 (92.5–122.7)	102.1 (87.3–116.9)	12.13%	<0.01
Preop CKD 2	76.4 (71.9–80.9)	80.3 (72.7–87.9)	77.6 (69.2–85.9)	1.57%	0.67^a
Preop CKD 3 to 5	42.5 (31.6–53.4)	39.3 (28.3–50.3)	39.5 (28.9–50.2)	7.05%	0.03
Mean eGFR in mL/min all patients (95% CI)	87.3 (80.4–94.2)	82.1 (75.3–88.9)	81.6 (75.5–87.7)	6.52%	<0.01

Statistical analysis underpowered to find difference.

eGFR=estimated glomerular filtration rate; LPN=laparoscopic partial nephrectomy; CI=confidence interval; preop=preoperative; CKD=chronic kidney disease; LAT=laparoscopic ablative therapy.

The LAT and LPN groups were subdivided based on preoperative CKD status, and further analysis was performed. When evaluating functional changes from baseline to 12-month follow-up, the most significant decreases were found for persons with baseline function greater than 90 mL/min, 117.9 to 106.7 mL/min (P<0.01) and 116.2 to 102.1 mL/min (P<0.01) for LPN and LAT, respectively. Other comparisons are limited because of a lack of power to detect difference.

The mean percent decline of eGFR from baseline to 12-month follow-up was similar between groups (5.2% LPN and 8.3% LAT (P=0.971)). Similarly, no difference in percent decline of eGFR from baseline to 12 months was seen when comparing treatment modality and taking preoperative CKD status into account.

Complications

The overall complication rate was similar for both groups (P=0.47). The number of patients who experienced intraoperative complications, however, tended to be greater for the LPN group (5) vs LAT (1) (P=0.18). Conversely, there were fewer postoperative complications for LPN (6) vs LAT (12) (P=0.11). The most common complication for all groups was hemorrhage. No conversion from laparoscopic to an open technique was performed for LAT. There were four conversions to open for LPN (P=0.11). Postoperative complications were further classified using the Clavien-Dindo system.¹⁷ In total, 3 grade I and 9 grade 2 complications occurred in the LAT group and 1 grade I and 5 grade II complications occurred in the LPN group. No grade III or higher complications occurred. A summary of all complications encountered can be found in Table 6.

Table 6.

Summary of Complications

Intraoperative complication	Number LAT	Number LPN	Clavien-Dindo grade
Retroperitoneal hematoma	1
Hemorrhage necessitating transfusion		2
Vascular injury with primary repair		2
Injury to viscus organ with primary repair		1
Postoperative complication (<30 days)
Epigastric pain	2		I
Urinary retention	1		I
Incisional hernia not necessitating intervention		1	I
Deep venous thrombus	1		II
Hemorrhage necessitating transfusion	6	3	II
Volume overload necessitating medical treatment	2	1	II
Urinary tract infection		1	II

LAT=laparoscopic ablative therapy; LPN=laparoscopic partial nephrectomy.

Discussion

While the gold standard treatment for patients with SRMs is PN, LAT is performed more commonly than LPN for patients who are older, with smaller tumors, with baseline renal insufficiency, and are poor operative candidates.^6,18 This bias toward LAT stems from the belief that LAT in comparison with LPN is associated with less morbidity and perhaps better long-term renal function because hilar clamping is not needed; moreover, LAT may be less challenging surgically than LPN. Few matched comparisons of LAT and LPN have been performed, however.

Our cohort had no statistically significant difference in most patient characteristics. There was a significant difference in mass characteristics, with LPN having a greater proportion of endophytic and lower pole tumors. This is likely secondary to surgeon bias with regard to case selection. In our experience, locating and achieving adequate ablation for completely endophytic tumors can be difficult, even with the use of ultrasound; thus, a tendency to manage with excision. Similarly, lower pole tumors are comparatively easier to manage with excision than upper pole or midpolar tumors, which may account for an increased use of LPN.

Despite the increased technical difficulty that is associated with LPN, the morbidity that is associated with both procedures was not significantly different in the hands of expert surgeons. In the hands of less experienced laparoscopists, an advantage with LAT may be demonstrable. In the future, the use of minimally invasive PN may become more commonplace among patients with SRMs as more surgeons overcome the technical challenges of LPN with the adoption of robotics.¹⁹ The percent decline in renal function that was observed in both groups did not differ. LPN was associated with longer operative time and higher EBL (151 mL vs 54 mL) compared with LAT, which is congruent with similar studies.^13,14,20

Our institution does not offer a percutaneous approach for ablative treatments of renal masses. The percutaneous ablative approach has been shown to be associated with less morbidity in comparison with LPN.¹² A laparoscopic approach to ablative therapies is still necessary when the tumor location is not amenable to a percutaneous approach. Furthermore, many of the complications that are associated within both groups are directly related to the process of ablation or tumor excision rather than the use of a laparoscopic approach.

No significant difference was seen in eGFR between treatment groups preoperatively, postoperatively, and at 12-month follow-up. A precipitous drop in eGFR resulting in a new dialysis requirement was not seen in patients from either group at or before 12-months follow-up. There was, however, a significant decrease of eGFR within each treatment group that occurred postoperatively and persisted. In our subset analysis, it appears that this change in eGFR was most significant for patients with stage 1 CKD for both LPN and LAT. There was also a decrease in eGFR for LAT with preoperative CKD status of 3 or less. While small, the long-term significance of this drop cannot be determined.

O'Malley and colleagues²⁰ performed the only matched cohort study comparing LPN with laparoscopic cryoablation. This study consisted of 30 patients, 15 in each arm. While the patient population was small, the overall clinical outcome between groups was similar to our findings in that the two groups had similar complication rates, length of stay, and changes in creatinine level and Hct.²⁰ Long-term assessment of renal function and oncologic assessment were not performed.

Within our study, the proportion of patients with benign tissue was found to be significantly higher for LAT than those treated with LPN. The pathologic findings in the LAT group were based solely on laparoscopic biopsy, while the entire resected specimen was evaluated for the LPN group. Therefore, it is likely that the differences are because of technical limitations of laparoscopic biopsy rather than an inherent difference in tumors. These findings elucidate a known limitation of renal mass biopsy during ablative techniques and are not unique to our study.¹² In the future, obtaining multiple biopsies at the time of ablation will be strongly considered to help ensure adequate tumor sampling.

Patients who underwent LAT had an increased length of follow-up compared with LPN. This may be attributed to the surgeons' preference of more rigorous monitoring for patients who have received ablative treatment. To date, there is no consensus on the definition of radiographic recurrence or on follow-up imaging intervals after renal mass ablation.^21,22

Other studies have determined short-term oncologic control with LAT to be a viable strategy for both cryotherapy and RFA.²³ In an analysis that compared laparoscopic cryotherapy with open PN, Klatte and associates²⁴ showed similar complication rates in both groups; however, ablation was associated with a significantly higher rate of recurrence.²⁴ The authors therefore recommended a more conservative use of cryoablation. These results are similar to other studies showing ablative therapy to carry a higher risk of local recurrence, although similar rates of metastatic diseas.²⁵

Our study does have several limitations. It is a retrospective review of a relatively small group of patients. The choice to perform LAT or LPN was also dependent on surgeon and patient preference, and so an inherit bias does exist when comparing these groups retrospectively. Unlike similar studies, however, we only performed the procedures via a laparoscopic approach, and our patient groups were well matched. Longer follow-up will also be necessary to determine oncologic control. Despite the limitations, we think our study shows that similar clinical and functional outcomes can be achieved for LPN vs LAT in the hands of experienced laparoscopic surgeons.

Conclusion

To compare the functional outcome between patients undergoing LPN and LAT, a pairwise matched controlled study was performed. In view of our results showing similar morbidity and preservation of renal function between groups, we think that the use of LPN should be routinely considered for appropriate patients with a SRM.

Footnotes

Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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