Tailoring Technique of Laparoscopic Partial Nephrectomy to Tumor Characteristics

Tailoring Technique of Laparoscopic Partial Nephrectomy to Tumor Characteristics Alon Z. Weizer, Scott M. Gilbert, William W. Roberts, Brent K. Hollenbeck and J. Stuart Wolf, Jr.*,† From the Divisions of Urologic Oncology (AZW, SMG, BKH, JSW), Minimally Invasive Surgery (AZW, WWR, BKH, JSW) and Health Services Research (SMG, BKH), Department of Urology, University of Michigan, Ann Arbor, Michigan

Purpose: We use a tailored approach to laparoscopic partial nephrectomy based on tumor depth of penetration and proximity to the renal sinus. We evaluated differences in perioperative outcomes to determine the value of this paradigm. Materials and Methods: The surgical approach to hilar clamping and tumor bed management during laparoscopic partial nephrectomy included no clamp or suture, clamp with no suture, and clamp and suture. The end points assessed retrospectively were differences in perioperative, pathological and complication outcomes among these groups. Results: Our surgical paradigm was used in 174 patients, including no clamp or suture in 36, clamp with no suture in 25, and clamp and suture in 113. Compared to the other patients those with a clamp and suture procedure were older with larger and deeper tumors that were closer to the renal sinus-collecting system and more likely to be malignant. Operative time was shortest in the no clamp or suture group and in the 2 clamp groups warm ischemia and operative times were shorter than in the no suture group. Estimated blood loss, hospital stay, surgical margins, complications and recurrences did not differ among the groups. A creatinine increase of 0.3 mg/dl or greater was seen in 33 patients (19%) following surgery, which was attributable to conversion to nephrectomy in 4, contralateral nephrectomy or partial nephrectomy in 3 and underlying medical renal disease in 1. In the remaining 25 patients no other cause was apparent except renal hilar clamping and tumor resection. Conclusions: A tailored approach based on tumor location and proximity to the renal sinus-collecting system can limit operative and ischemia times, and technically simplify the procedure without adversely impacting morbidity, convalescence and oncological outcomes. Key Words: kidney neoplasms, nephrectomy, laparoscopy, surgical instruments, sutures

aparoscopic approaches to benign and malignant renal diseases can decrease the severity and duration of postoperative convalescence without compromising outcomes. With the acceptance of laparoscopic nephrectomy as a standard of care1,2 laparoscopic partial nephrectomy is increasing as an alternative surgical option3,4 with promising early outcomes.5 To date the technique of laparoscopic partial nephrectomy includes a wide variety of hemostatic options.6 Traditionally open partial nephrectomy has been performed with hypothermia in cases of prolonged renal ischemia, meticulous sutured closure of blood vessels and collecting system entry, and sutured management of the tumor bed.7 A great deal of effort has been spent on identifying novel methods to replicate these steps using a laparoscopic approach.8 –10 However, a number of technological advances potentially obviate some of these traditional maneuvers for open and laparoscopic partial nephrectomy without compromising

L

Submitted for publication February 24, 2008. Study received institutional review board approval. * Correspondence: 3875 Taubman Center, 1500 East Medical Center Dr., Ann Arbor, Michigan 48109-0330 (FAX: 734-936-9127; e-mail: [email protected]). † Financial interest and/or other relationship with Terumo and Omeros. To view the accompanying video, please see the online version of this article (Volume 180, Number 4) at www. jurology.com.

0022-5347/08/1804-1273/0 THE JOURNAL OF UROLOGY® Copyright © 2008 by AMERICAN UROLOGICAL ASSOCIATION

outcomes. The impact of kidney removal on long-term renal function11,12 along with the convalescence benefit of laparoscopy1 should encourage clinicians to explore ways to perform laparoscopic partial nephrectomy effectively and safely. Based on our initial experience with laparoscopic partial nephrectomies13 we have developed a tailored approach to renal hilum and tumor bed management based on penetration depth and proximity to the renal sinus-collecting system that does not require renal hilar clamping and parenchymal suturing in all patients. We evaluated the impact of this algorithm on the outcomes of laparoscopic partial nephrectomy at our institution.

METHODS Patient Identification and Group Stratification Using our institutional review board approved laparoscopic database we identified 249 patients who underwent laparoscopic partial nephrectomy through April 2007. We excluded our first 75 patients (before October 2003), who underwent surgery before the implementation of our current treatment algorithm. Results in these patients and the rationale for developing our selective surgical technique have been previously described (see video segment).13,14 A total of 174 patients operated on by 3 surgeons (JSW, BKH and WWR) was evaluated. Based on tumor depth of penetration into the renal parenchyma and proximity to the renal sinus-collect-

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Vol. 180, 1273-1278, October 2008 Printed in U.S.A. DOI:10.1016/j.juro.2008.06.066

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ing system we developed an algorithm for selective hilar clamping and sutured management of the tumor bed (see figure). In our experience renal hilar clamping is needed only when renal ischemia is required to control intraoperative blood loss and improve visualization during resection, while a sutured bolster is required only when the renal sinuscollecting system is entered. For tumors with less than 5 mm penetration into the renal parenchyma the hilum is not clamped, although it is identified and a window of dissection is created in case clamping is required. The tumor bed is then managed by argon beam coagulation and hemostatic agents. FloSeal™ is routinely used based on a prior porcine study performed by our group.6 For tumors with more than 5 mm penetration but that are still more than 5 mm from the sinus-collecting system a clamp is placed on the renal hilum with continued tumor bed management with argon beam coagulation and hemostatic agents. Tumors within 5 mm of the renal sinus or collecting system generally require hilar clamping and a sutured bolster secondary to the increased likelihood of renal sinus-collecting system entry. Although the algorithm is driven by measurements made from computerized tomography, the final decisions are made intraoperatively with the assistance of surface ultrasonography. Data Abstraction Demographic information, medical history, operative details, preoperative cross-sectional imaging details, pathology results, including pathological stage based on the 2002 American Joint Committee on Cancer/UICC TNM pathological staging system, and the change in creatinine, based on preoperative and the most recent measurement with the date determined, were abstracted from the database. Spe-

cific complications, their timing, the organ system involved and grade using the 5-tiered scale based on National Cancer Institute Common Toxicity Criteria (http://ctep.cancer.gov/ forms/CTCAEv3.pdf) were obtained for each patient. Postoperative hemorrhage was defined as an acute decrease in hematocrit and/or a need for red blood cell transfusion not accounted for by intraoperative blood loss. All complications reported within 30 days and those directly related to surgery beyond 30 days were included. Followup, recurrence and progression were determined by the date of the last crosssectional imaging. Analysis Our exposure variable was the approach to the renal hilum and tumor bed, including 1) no hilar clamping or sutured bolster of the tumor bed, ie no clamp or suture, 2) hilar clamping without sutured bolster of the tumor bed, ie clamp with no suture, and 3) hilar clamping with sutured bolster of the tumor bed, ie clamp and suture. Differences in outcomes among the 3 groups were assessed using commercial statistical software. For categorical variables the chi-square or Fisher exact test was used to assess significance. For continuous variables the Kruskal-Wallis test or the MannWhitney U test for 2 groups was used to compare groups. Post hoc testing was performed to assess pairwise differences in groups with significant differences using the Bonferroni correction. All statistical tests were 2-sided and performed at a significance level of ⬍0.05. RESULTS Based on our paradigm 36, 25 and 113 patients were in the no clamp or suture, clamp with no suture, and clamp and

Algorithm for managing renal masses amenable to laparoscopic partial nephrectomy

TAILORING LAPAROSCOPIC PARTIAL NEPHRECTOMY TO TUMOR CHARACTERISTICS

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TABLE 1. Demographic and clinical variables Overall No. pts No. sex (%) M F Median age (range) No. American Society of Anesthesiologists score (%): 1–2 3–4 Median kg/m2 body mass index (range) No. mass site (%): Rt Lt Bilat Median cm mass size (range) No. mass kidney site (%): Upper Interpolar Lower Median mm mass penetration depth (range) Median mm mass–renal sinus distance (range) No. solitary kidney (%) Median ng/ml baseline creatinine (range)

No Clamp, No Suture

174

Clamp, No Suture

36

25

Clamp ⫹ Suture

p Value

113

105 69 59

(60) (40) (29–89)

20 16 57

(56) (44) (30–89)

16 9 53

(64) (36) (34–82)*

69 44 62

(61) (39) (29–84)*

123 50 29

(71) (29) (18–67)

22 13 29

(63) (37) (18–50)

18 7 29

(72) (28) (18–67)

83 30 29

(73) (27) (19–54)

0.48

(37) (63)

0.25

70 103 1 2.4 45 58 68 12 5 5 1

(40) (59) (1) (1–9)

17 18 1 1.9

(26) (34) (40) (0–70) (0–62) (3) (0.6–2.8)

8 15 12 5 17 3 1

(47) (50) (3) (1–9)

11 14 0 1.9

(23) (43) (34) (0–7)* (0–62)*,‡ (8) (0.6–2.0)

5 14 6 9 13 0 1

(44) (56)

42 71 0 2.6

(1–4)* (20) (56) (24) (6–15)† (5–23)*,†

32 29 50 16 0 2 1

(0.7–2.0)

(1–7)* (29) (26) (45) (2–30)*,† (0–16)†,‡ (2) (0.6–2.8)

0.78 0.04

0.57

⬍0.01 0.04 ⬍0.01 ⬍0.01 0.08 0.81

*,†,‡ Pairs with post hoc significance testing ⬍0.05.

No differences in estimated blood loss, the reexploration rate, conversion to open surgery or the need for nephrectomy existed among the 3 groups. Seven patients underwent conversion to nephrectomy (laparoscopic in 5 and open in 1) or open surgical partial nephrectomy. Three conversions to nephrectomy occurred in the no clamp or suture group. In 1 case a positive margin on frozen section prompted nephrectomy without residual tumor in the nephrectomy specimen. In another case radical nephrectomy was elected when multiple renal masses were found intraoperatively. In the remaining case, which accounted for the greatest blood loss in our series of 3,500 ml, urgent conversion to open surgical radical nephrectomy was necessitated by renal vein injury during initial balloon dilation of the retroperitoneal space. Thus, of the 3 patients with no clamp or suture included as having undergone conversion to radical nephrectomy, partial nephrectomy was attempted in only 1 and in that patient the decision to convert was based on concern for residual tumor, which proved to be incorrect. The other 2 cases were included in our analysis because they accurately rep-

suture groups, respectively. Age in the clamp and suture group was greater than in the clamp with no suture group (median 62 vs 53 years, p ⫽ 0.04). Significant differences in median tumor size, depth of tumor penetration and proximity to the renal sinus confirmed the application of our algorithm (table 1). Most procedures were performed transperitoneally. However, a retroperitoneoscopic approach was used in 40% of clamp with no suture cases compared to 25% of no clamp and no suture, and 14% of clamp and suture cases. Mean ⫾ SD operative time was 222 ⫾ 44, 196 ⫾ 55 and 157 ⫾ 44 minutes in the hand assisted, transperitoneal and retroperitoneal partial nephrectomy groups, respectively (p ⬍0.01). There was a significant difference in operative time among all study groups with the shortest procedures in the no clamp or suture group and the longest procedures in the clamp and suture group (median 142 vs 200 minutes) (table 2). When hilar clamping was done, there was significantly greater warm ischemia time in suture than in no suture cases (median 30 vs 13 minutes).

TABLE 2. Perioperative data Overall No. pts No. surgical approach (%): Hand assisted laparoscopic nephrectomy Transperitoneal Retroperitoneal Median mins operative time (range) Median mins warm ischemia time (range) Median ml estimated blood loss (range) No. reexploration (%) No. conversion (%) No. nephrectomy (%) Median days hospital stay (range) No. mg/dl creatinine change from baseline (%): 0 Greater than 0–0.2 Greater than 0.2–0.4 Greater than 0.4 *,† Pairs with post hoc significance testing ⬍0.05.

No Clamp, No Suture

174

36

40 (23) 99 (57) 35 (20) 188 (84–346) 29.2 (8.0–86.0) 200 (0–3,500) 1 (1) 7 (4) 6 (3) 2 (1–61) 92 43 19 14

(55) (26) (11) (8)

25

9 (25) 18 (50) 9 (25) 142 (84–274)* Not applicable 175 (0–3,500) 1 (3) 3 (8) 3 (8) 2 (1–11) 23 6 2 2

Clamp, No Suture

(70) (18) (6) (6)

p Value

113

0 15 (60) 10 (40) 160 (100–243)† 13.2 (8.0–23.2) 100 (25–1,200) 0 1 (4) 1 (4) 2 (1–6) 11 6 4 3

Clamp ⫹ Suture

(46) (25) (17) (12)

31 (27) 66 (58) 16 (14) 200 (107–346)*,† 30.3 (10.0–86.0) 200 (10–1,900) 0 3 (3) 2 (2) 2 (1–61) 58 31 13 9

(52) (28) (12) (8)

⬍0.01 ⬍0.01 ⬍0.01 0.25 0.15 0.32 0.17 0.20 0.66

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resent our experience on an intent to treat basis. In 2 of the 3 patients in the clamp groups who underwent conversion to radical nephrectomy conversion was done for poor hemostasis after unclamping the hilum and in 1 it was done for a positive margin on frozen section but, again, there was no tumor in the nephrectomy specimen. The final conversion in our series was to open surgical partial nephrectomy in a patient in the clamp with suture group when a lower pole artery of a functionally solitary kidney required repair after injury. The mean creatinine change was 0.11 ⫾ 0.23 mg/dl in the no clamp or suture group, 0.17 ⫾ 0.25 mg/dl in the clamp with no suture group and 0.17 ⫾ 0.43 mg/dl in the clamp and suture group at a mean followup of 10, 12 and 12 months, respectively (p ⫽ 0.66). A total of 33 patients (19%) had a 0.3 or greater creatinine increase following surgery, including 4 (11%) in the no clamp or suture group and 29 (21%) in the clamp groups. This greater increase in creatinine than anticipated was explained by conversion to nephrectomy in 4 patients, contralateral or partial nephrectomy before or after laparoscopic partial nephrectomy in 3 and baseline medical renal disease in 1. The creatinine increase in all 4 patients with no clamp was associated with 1 of these factors. There was no apparent cause of the creatinine increase other than partial nephrectomy with hilar clamping in the remaining 25 patients, representing 18% of patients with clamping. Average baseline creatinine was 1.0 ⫾ 0.3 mg/dl in patients without a 0.3 mg/dl or greater increase in creatinine postoperatively compared to 1.2 ⫾ 0.3 mg/dl in those without other mitigating circumstances to explain an increase in postoperative creatinine (each was within our normal institutional range). This compared to a mean creatinine of 1.5 ⫾ 0.3 mg/dl in patients with mitigating circumstances to explain the creatinine increase. Overall 35% of patients experienced a minor complication and 6% experienced a major complication (table 3). No difference existed among the study groups. Urine leakage or postoperative hemorrhage developed in 3% and 8% of patients, respectively. A total of 87 complications were identified in the entire cohort of patients. Using the Common Terminology Criteria for Adverse Events reporting system 86% of complications were grade 1 or 2 with only 1 patient experiencing a grade 4 complication. There were no grade 5 complications. Most complications reported were early (during hospitalization) and urological in origin, including urinary tract infection, hematuria, urine leakage, hemorrhage and urinary retention (data not shown). Table 4 lists pathological and followup data. Patients with a clamp and suture procedure had larger specimens and tumors. Only 44% of the patients in the no clamp or suture group had malignant tumors but of the last 25 in the

no clamp or suture group 75% had malignant tumors, perhaps reflecting our growing use of observation and percutaneous biopsy for small renal masses. There were no differences in the frequency of final positive surgical margins among the groups. Of the 130 of 174 patients (75%) with malignant tumors we have followup on 79 with a median duration of 14 months (range 1.8 to 40) and no recurrences. DISCUSSION This study builds on our initial experience with laparoscopic partial nephrectomy, during which we found that tumor resection entering the renal sinus was associated with an unacceptably high rate of hemorrhage and urinary leakage when a sutured bolster was not used.13 In this study we report that omitting renal hilar clamping and the sutured bolster during laparoscopic partial nephrectomy in select patients did not increase blood loss, complications or the frequency of positive surgical margins. Of our patients 65% required renal hilar clamping and a sutured bolster but we safely omitted the sutured bolster in 35% and hilar clamping in 21%. The important question is what is gained by avoiding renal hilar clamping or a sutured bolster. Omitting hilar clamping decreases operative time and avoids ischemia without increasing blood loss or the final positive surgical margins. When hilar clamping is required, avoiding a sutured bolster decreases operative time and decreases ischemia time. While our study does not demonstrate a significant difference among the groups in the overall creatinine increase from baseline, an increase of 0.3 mg/dl or greater with no explanation other than partial nephrectomy occurred only in patients with hilar clamping. This difference is substantiated by the fact that baseline creatinine was similar in patients without an increase and in those with an increase explained by hilar clamping alone. In a recent series the rate of renal unit loss following laparoscopic partial nephrectomy was 2.1%.5 Avoiding a hilar clamp decreases the risk of renal artery injury which, although rare, can result in significant complications, including malignant hypertension.15 This risk is disproportionate, given the fact that 56% of these small tumors in our series that did not require a hilar clamp were benign and posed little risk to the patient. Are these benefits enough to advocate no clamp or suture in select patients when our results demonstrate no difference in terms of blood loss, conversion to nephrectomy, complications and pathological outcomes compared to those of partial nephrectomy with hilar clamping? While there were no statistical differences among groups, the absolute numbers demonstrate that patients without hilar clamping com-

TABLE 3. Complication data Complications Overall Specific: Urine leakage Postop hemorrhage Overall: Any Major Minor

No. Pts (%) 174

No. No Clamp, No Suture (%) 36

No. Clamp, No Suture (%) 25

No. Clamp ⫹ Suture (%)

p Value

113

6 (3) 14 (8)

1 (3) 2 (6)

0 2 (8)

5 (4) 10 (9)

0.53 0.81

63 (36) 10 (6) 59 (34)

12 (33) 2 (5) 12 (33)

5 (20) 0 5 (20)

46 (41) 8 (7) 42 (37)

0.14 0.47 0.24

TAILORING LAPAROSCOPIC PARTIAL NEPHRECTOMY TO TUMOR CHARACTERISTICS

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TABLE 4. Pathological results and followup data

No. pts Median cm specimen size (range) Median cm tumor size (range) Median cm specimen-tumor difference (range) No. Ca (%) No. histology (%): Clear cell Papillary Chromophobe Oncocytoma Angiomyolipoma Other benign No. final pos margin (%) Median mos followup (range)* No. stage (%): T1a T1b T2 T3a No. local recurrence or metastasis (%)

Overall

No Clamp, No Suture

Clamp, No Suture

174 3.5 (1–21) 2.3 (0.1–9) 1.3 (0–15) 130 (75)

36 2.5 (1–21) 1.6 (0.1–9)† 1.3 (0–15) 16 (44)

25 2.5 (2–9)* 1.8 (1–4)* 1.2 (0–7) 20 (80) 15 5 0 3 2 0 2 13

91 33 6 25 7 12 6 14

(52) (19) (3) (14) (4) (7) (3) (1.8–40)

13 3 0 7 3 10 0 12

109 13 1 6 0

(85) (10) (1) (5)

11 2 1 1 0

(36) (8) (19) (8) (28) (3–36) (73) (13) (7) (7)

19 0 0 1 0

(60) (20) (12) (8) (8) (4–31) (95) (5)

Clamp ⫹ Suture 113 3.5 2.5 1.2 94

(2–15)* (1–6)*,† (0–12) (83)

p Value ⬍0.01 ⬍0.01 0.63 ⬍0.01

63 25 6 15 2 2 4 17

(56) (22) (5) (13) (2) (2) (4) (1.8–40)

⬍0.01

79 11 0 4 0

(84) (12)

0.10

(4)

0.31 0.61

⬎0.99

*,† Pairs with post hoc significance testing ⬍0.05. ‡ In 79 patients with malignant histology based on physical examination, chest x-ray and 3-dimensional axial imaging.

pared to the clamp and suture group had an estimated median blood loss of 175 vs 200 ml, less frequent postoperative hemorrhage (6% vs 9%), a decreased incidence of urine leakage (3% vs 4%), fewer complications (major complications 5% vs 7%) and fewer final positive surgical margins (0% vs 4%). The small number in each group and the variability of the statistic may have limited our ability to detect a difference that actually existed. In addition, the published literature on laparoscopic partial nephrectomy without hilar clamping using various hemostatic instruments shows that an average of 10% of patients experience hemorrhage and 10% experience urine leakage.16 –20 Our 6% hemorrhage rate and 3% urine leakage rate in the no clamp or suture group compares favorably to these values and demonstrates the impact of our algorithm on identifying appropriate patients in whom to avoid hilar clamping. The greater number of nephrectomies performed in the no clamp and suture group reflects our use of intent to treat analysis, rather than the exclusion of patients in whom intraoperative findings prompted nephrectomy. If these patients were excluded, only 2 nephrectomies would have been performed in this series, which is similar to values in the reported literature. Finally, differences among groups may have been attenuated by the fact that, despite the small tumor size, patients in the no clamp or suture group were more likely to have a solitary kidney and a greater proportion were in American Society of Anesthesiologists class 3 or 4. Each factor is suggestive of greater medical comorbidities. Combined with the stated advantages these data suggest that no clamp or suture should be considered in select patients. Not all renal masses are amenable to a no clamp or suture approach. For our algorithm to be applicable a dedicated computerized tomography image of the renal mass with thin slices must be evaluated to assess the depth of tumor penetration into the kidney and proximity to the renal sinus. Even when imaging suggests a shallow lesion, the surgeon should dissect the renal hilum (a core skill for laparoscopic radical nephrectomy) and confirm the approach with intraoperative ultrasound. The surgical plan should be dynamic, considering intraoperative findings or technical

challenges that may necessitate conversion to hand assisted or open surgical partial or radical nephrectomy depending on clinical circumstances. In addition, the decision to suture is made after tumor resection so that, if a surgeon is not prepared to suture, it would be prudent to avoid borderline lesions. Lesions between 5 and 10 mm from the renal sinus on imaging are occasionally associated with resections that enter the renal sinus-collecting system and, therefore, would benefit from sutured bolster placement according to our algorithm. Despite the results of our study there are several limitations that deserve mention. This series is primarily based on the efforts of 1 surgeon and the results may not be generalizable. However, rather than summarizing the results of a skilled surgeon using only advanced techniques, this study demonstrates a practical approach to laparoscopic partial nephrectomy for surgeons with a less extensive laparoscopic background. Additionally, this study may be subject to selection bias because patients were counseled and offered alternatives, including open partial nephrectomy, observation, ablative techniques and pretreatment biopsy, and they elected laparoscopic partial nephrectomy, potentially creating a nonrepresentative population. However, our patient characteristics are similar to those in other reported series.

CONCLUSIONS Laparoscopic partial nephrectomy can be tailored to tumor characteristics. Avoiding a hilar clamp decreases operative time and avoids renal ischemia without increasing blood loss or the frequency of positive surgical margins. Using a hilar clamp combined with hemostatic agents and argon beam coagulation without a sutured bolster decreases operative and ischemia times without compromising pathological and complication parameters. Finally, laparoscopic partial nephrectomy with a hilar clamp and a sutured bolster allows the management of larger tumors via a laparoscopic approach with outcomes similar to those anticipated for open surgical partial nephrectomy.

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