A Matched Comparison of Perioperative Outcomes of a Single Laparoscopic Surgeon Versus a Multisurgeon Robot-Assisted Cohort for Partial Nephrectomy

A Matched Comparison of Perioperative Outcomes of a Single Laparoscopic Surgeon Versus a Multisurgeon Robot-Assisted Cohort for Partial Nephrectomy Jonathan S. Ellison, Jeffrey S. Montgomery, J. Stuart Wolf, Jr., Khaled S. Hafez, David C. Miller and Alon Z. Weizer* From the Department of Urology, University of Michigan, Ann Arbor, Michigan

Purpose: Minimally invasive nephron sparing surgery is gaining popularity for small renal masses. Few groups have evaluated robot-assisted partial nephrectomy compared to other approaches using comparable patient populations. We present a matched pair analysis of a heterogeneous group of surgeons who performed robot-assisted partial nephrectomy and a single experienced laparoscopic surgeon who performed conventional laparoscopic partial nephrectomy. Perioperative outcomes and complications were compared. Materials and Methods: All 249 conventional laparoscopic and robot-assisted partial nephrectomy cases from January 2007 to June 2010 were reviewed from our prospectively maintained institutional database. Groups were matched 1:1 (108 matched pairs) by R.E.N.A.L. (radius, exophytic/endophytic properties, nearness of tumor to collecting system or sinus, anterior/posterior, location relative to polar lines) nephrometry score, transperitoneal vs retroperitoneal approach, patient age and hilar nature of the tumor. Statistical analysis was done to compare operative outcomes and complications. Results: Matched analysis revealed that nephrometry score, age, gender, tumor side and American Society of Anesthesia physical status classification were similar. Operative time favored conventional laparoscopic partial nephrectomy. During the study period robot-assisted partial nephrectomy showed significant improvements in estimated blood loss and warm ischemia time compared to those of the experienced conventional laparoscopic group. Postoperative complication rates, and complication distributions by Clavien classification and type were similar for conventional laparoscopic and robot-assisted partial nephrectomy (41.7% and 35.0%, respectively). Conclusions: Robot-assisted partial nephrectomy has a noticeable but rapid learning curve. After it is overcome the robotic procedure results in perioperative outcomes similar to those achieved with conventional laparoscopic partial nephrectomy done by an experienced surgeon. Robot-assisted partial nephrectomy likely improves surgeon and patient accessibility to minimally invasive nephron sparing surgery.

Abbreviations and Acronyms CLPN ⫽ conventional laparoscopic partial nephrectomy EBL ⫽ estimated blood loss eGFR ⫽ estimated glomerular filtration rate ICU ⫽ intensive care unit LOS ⫽ length of stay RAPN ⫽ robot-assisted partial nephrectomy SRM ⫽ small renal mass WIT ⫽ warm ischemia time Submitted for publication October 17, 2011. Study received institutional review board approval. * Correspondence: 7312 CCC, 1500 East Medical Center Dr., SPC 5946, Ann Arbor, Michigan 48109 (telephone: 734-615-8829; FAX: 734-6479480).

Key Words: kidney, kidney neoplasms, nephrectomy, laparoscopy, robotics THERE has been a dramatic increase in robotic assistance for SRMs. Large case series have established the oncological safety and improved convalescence of laparoscopic partial nephrectomy com-

pared to open partial nephrectomy in appropriately selected patients.1–3 It is likely that the benefits of laparoscopic partial nephrectomy can be extended to the robotic platform but to our knowl-

0022-5347/12/1881-0045/0 THE JOURNAL OF UROLOGY® © 2012 by AMERICAN UROLOGICAL ASSOCIATION EDUCATION

Vol. 188, 45-50, July 2012 Printed in U.S.A. DOI:10.1016/j.juro.2012.02.2570

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SINGLE LAPAROSCOPIC SURGEON VERSUS MULTISURGEON ROBOT-ASSISTED NEPHRECTOMY

edge it is unknown whether there are any evident advantages of the robotic over the laparoscopic approach. Partial nephrectomy is underused even in patients with SRMs 2 cm or less, who are more likely to undergo laparoscopic radical nephrectomy than nephron sparing surgery.4 The unique technology of the robotic platform, eg wristed instrumentation and 3-dimensional, high definition magnified vision, may make nephron sparing approaches more readily available to urological surgeons and expand minimally invasive management to more difficult tumors. However, current data are limited to small reviews or single surgeon series.5,6 Also, comparisons of surgical techniques for renal cancer have been limited by the lack of a standardized description of SRMs. Bias may be introduced in comparative reviews since the surgical approach is often influenced by the perceived difficulty of resection. Recently introduced scoring systems for renal mass complexity have the potential to allow more meaningful comparisons of surgical options.7,8 We present a matched comparison between a multisurgeon RAPN cohort and a single surgeon laparoscopic partial nephrectomy cohort using the R.E.N.A.L. nephrometry scoring system for matching to control for tumor difficulty.8

METHODS All patients treated with CLPN or RAPN for suspected malignancy from January 2007 to January 2011 were identified in our single institution, prospectively maintained, institutional review board approved database. The CLPN cohort included only cases performed by a single, experienced laparoscopic surgeon (JSW) and excluded those requiring hand assistance. RAPN was performed by 5 attending surgeons using the da Vinci® Surgical System. Nephrometry scores were determined by retrospective review of imaging by urological surgeons before May 2010 and were captured prospectively thereafter. If imaging was unavailable, the case was excluded from analysis. Demographic and patient characteristics, perioperative information and pathological data were abstracted from the prospectively maintained database. We calculated eGFR using the modification of diet in renal disease formula.9 The nephrometry scoring system was used as previously described by Kutikov and Uzzo.8 Tumors were stratified into groups, including low— 4 to 6, moderate—7 to 9 and high—10 to 12 points. Hilar tumors are defined as masses that touch the renal vessels. Complications were stratified by severity, as defined by the Clavien classification, and by type.10 Hemorrhagic complications were defined as those necessitating blood transfusion for intraoperative or postoperative blood loss, or those involving clinically significant bleeding, ie hematuria, requiring further management. Early (within 30 days) and late (30 to 90 days) complications were included in analysis. One-to-one matching was done between the CLPN and RAPN groups by nephrometry score (low, intermediate or

high), transperitoneal vs retroperitoneal approach, hilar location and patient age (⫾ 15 years). Intraoperative conversions to nephrectomy were excluded from study, including 1 CLPN converted due to hemorrhage and 3 RAPNs converted for oncological control. To assess the effects of a learning curve on results with time patients in each group were stratified by operation date at 3-month intervals and regression curves were constructed. Statistical analysis was done to compare preoperative patient and tumor characteristics, perioperative outcomes and complications using SAS®, version 9.2. When applicable, paired statistical analysis was done. Mean values were used for all continuous variables and the paired t test was used for statistical analysis. For categorical variables the McNemar test or ␬ statistics were applied for comparison. No adjustment was made for multiple statistical tests, although all tests were hypothesis driven. Statistical significance was considered at p ⬍0.05.

RESULTS A total of 145 RAPNs and 204 CLPNs were performed at our institution from January 2007 to June 2011, of which 19 CLPN and 14 RAPN cases were excluded from study due to incomplete imaging, pathological or laboratory data. Ten CLPN cases performed by another surgeon and 34 hand assisted laparoscopic cases were also excluded. Acceptable matches were obtained for the 108 patients remaining in each group. Our data pooled the results of a single experienced laparoscopic surgeon and 5 robotic surgeons who performed minimally invasive nephron sparing surgery. The CLPN surgeon had extensive laparoscopic experience spanning more than 200 CLPNs and more than 1,000 laparoscopic procedures by 2007. Conversely the RAPN series included the first RAPN procedures done by 5 surgeons. The highest volume surgeon in the RAPN group accounted for 55% of the cases in this series. Table 1 lists preoperative patient and tumor characteristics. Significant differences were observed in patient age with a mean difference of 4 years between the CLPN and RAPN groups (55.9 vs 59.4 years, p ⬍0.0001). Anterior tumors were more common in the CLPN group while the RAPN group included more posterior tumors. The CLPN group included 6 patients with a solitary kidney compared to none in the RAPN group. Table 2 lists perioperative outcomes. There were differences between CLPN and RAPN in LOS (mean 2.2 vs 2.7 days, p ⫽ 0.02), WIT (mean 19.3 vs 24.9 minutes, p ⫽ 0.006) and operative time (mean 162 vs 215 minutes, p ⬍0.0001). In the CLPN and RAPN groups 34 and 8 patients, respectively, did not undergo renal hilar clamping. Excluding zero ischemia cases, WIT was comparable for CLPN and RAPN (mean 28.2 and 26.8 minutes, respectively, p ⫽ 0.46). Postoperative eGFR, the number of patients with eGFR less

SINGLE LAPAROSCOPIC SURGEON VERSUS MULTISURGEON ROBOT-ASSISTED NEPHRECTOMY

Table 1. Preoperative patient and tumor characteristics CLPN No. gender (%): M F No. side (%): Rt Lt Mean ⫾ SD age % American Society of Anesthesiologists score: 1–2 3–4 Mean ⫾ SD body mass index (kg/m2) Preop eGFR (ml/min/1.73 m2): Mean ⫾ SD No. less than 60 No. multifocal tumor (%) No. solitary kidney (%) Mean ⫾ SD tumor size (cm) Mean ⫾ SD invasion depth (mm) Mean ⫾ SD distance from sinus (mm) No. site (%): Anterior Posterior Neither anterior nor posterior No. nephrometry score (%): Low Intermediate High No. hilar (%)

RAPN

p value 0.057

62 (57) 46 (43)

66 (61) 42 (39)

57 (53) 51 (47) 55.9 ⫾ 10.6

52 (48) 56 (52) 59.4 ⫾ 12.1

33 67 29.3 ⫾ 6.1

39 61 30.9 ⫾ 6.5

0.057

85.8 ⫾ 2.4 11 6 (6) 6 (6) 2.7 ⫾ 1.4 14.2 ⫾ 7.3

81.4 ⫾ 2.0 19 4 (4) 0 2.9 ⫾ 1.6 14.7 ⫾ 8.4

0.905 0.06 0.53 ⬍0.0001 0.29 0.93

5.5 ⫾ 6.3

5.8 ⫾ 7.1

0.55

0.59

56 (52) 25 (23) 27 (25)

35 (49) 49 (45) 24 (22)

48 (44) 57 (53) 3 (3) 7 (7)

48 (44) 57 (53) 3 (3) 7 (7)

⬍0.0001 0.054

⬍0.0001

1

1

than 60 ml/minute/1.73 m2, the number in whom eGFR less than 60 ml/minute/1.73 m2 developed and transfusion requirements were similar in the groups. Of patients with assessable surgical margins positive surgical margins were identified in 7% with CLPN and 6% with RAPN (p ⫽ 0.7). The figure shows the mean trends of operative time, EBL, LOS and WIT with time for CLPN and RAPN with results stratified and plotted by 6-month intervals based on operation date. Comparison of the slope of the curve revealed significant differences between RAPN and CLPN for EBL (p ⫽ 0.01) and WIT (p ⫽ 0.03). Differences in operative time and LOS improved in a similar manner in the 2 groups, although this difference was not statistically significant. In the RAPN group improvements in WIT, EBL and operative time appeared to plateau at the 24-month point, by which time 33 RAPNs had been done. There was a total of 40 complications in 36 patients (33.3%) treated with CLPN and a total of 48 in 36 (33.3%) treated with RAPN. Four patients in the CLPN group experienced multiple complications compared to 8 in the RAPN group. There were 7 intraoperative complications in the RAPN (1 major and 6 minor) and 6 in the CLPN group (3 major and

47

3 minor). The minor complications of RAPN included renal hemorrhage requiring transfusion, hemorrhage from the vena cava and injury to the liver, which was managed robotically, in 1 case each and hemorrhage from unspecified sources, requiring transfusion, in 3. The major complication was an intraoperative bowel injury due to a malfunctioning Veress needle, which was managed robotically. The major complications of CLPN were ureteral injury, renal hemorrhage requiring take back for completion nephrectomy and renal vein injury in 1 case each, which were managed laparoscopically. Minor complications included hemorrhage from the resection site and 2 cases of unspecified hemorrhage, of which all required transfusion. The remaining reported complications developed postoperatively. The distribution of complications according to the Clavien grading system was similar for CLPN and RAPN (table 3). Most complications were minor (Clavien grade 1 or 2). Four complications of CLPN and 7 of RAPN were Clavien 3. Three complications of CLPN were grade 4a, including respiratory distress requiring ICU care in 2 patients and postoperative hemorrhage requiring emergent nephrectomy and postoperative ICU care in 1. The single 4a complication of RAPN was also respiratory distress requiring ICU care. There were no Clavien 4b or 5 complications in either group. The complication distribution by type was equal in the 2 groups (table 3). The category of other complications was the most common category in each group. These complications included ileus, urinary retention, urinary tract infection, gout flare, prolonged postoperative pain, constipation, diarrhea, Clostridium difficile infection, bowel perforation, renal ischemia, retroperitoneal hematoma, postoperative delirium and an obstructing clot in the renal

Table 2. Perioperative and oncological outcomes

Mean ⫾ SD EBL (ml) Mean ⫾ SD LOS (days) Mean ⫾ SD WIT (mins): Overall Excluding zero ischemia Mean ⫾ SD operative time (mins) Mean ⫾ SD postop eGFR (ml/min/1.73 m2) No. eGFR less than 60 ml/min/1.73 m2: Postop Developed postop No. transfusion (%) No. margin status (%): Pos Neg

CLPN

RAPN

p Value

400 ⫾ 580 2.2 ⫾ 1.2

368 ⫾ 430 2.7 ⫾ 1.9

0.63 0.02

19.3 ⫾ 17.8 28.2 ⫾ 14.5 162 ⫾ 55

24.9 ⫾ 11.9 26.8 ⫾ 9.5 215 ⫾ 47.3

0.006 0.46 ⬍0.0001

85.9 ⫾

2.4

81.0 ⫾

13 6 7 (7)

16 4 6 (6)

6 (7) 78 (93)

6 (7) 86 (93)

2.1

0.16

0.44 0.53 0.78 0.74

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SINGLE LAPAROSCOPIC SURGEON VERSUS MULTISURGEON ROBOT-ASSISTED NEPHRECTOMY

Perioperative outcome trends (dotted lines) for RAPH (red) and CLPN (blue) at 6-month intervals

collecting system. Urine leaks, acute kidney injury and nerve injury were rare. Table 4 lists the 11 patients with positive surgical margins, of which most were conventional clear cell renal cell carcinoma. Final pathological stage was T3a and T3b in 2 and 1 patients, respectively. Two patients with a final pathological stage of T3 underwent further intervention. In 1 patient in whom completion radical nephrectomy was done laparoscopically the final pathological evaluation of the

Table 3. Postoperative complications by Clavien score

Clavien score:* 1 2 3a 3b 4a Complication type:*,† Pulmonary Cardiac Wound Hemorrhage Urine leak Acute renal failure Other Nerve

No. CLPN (%)

No. RAPN (%)

40 20 (50) 13 (33) 2 (5) 2 (5) 3 (8) 40 5 (13) 1 (3) 4 (10) 9 (23) 4 (10) 0 16 (40) 1 (2)

48 14 (29) 26 (54) 4 (8) 3 (6) 1 (2) 48 4 (8) 4 (8) 4 (8) 9 (19) 2 (4) 2 (4) 23 (48) 0

* p ⫽ 0.32. † In each operative group 36 patients (33%) had complications (p ⫽ 0.88).

remnant kidney revealed pT0 disease. In the other patient local recurrence was diagnosed by cross-sectional imaging 26 months postoperatively, which was treated with percutaneous cryoablation. No difference in pathological tumor characteristics was observed in the 2 groups (table 5).

DISCUSSION We report a matched comparison between a single, experienced laparoscopic surgeon who performed CLPN and a heterogeneous group of robotic surgeons who performed RAPN early in their adoption of the robotic technique. LOS, WIT and operative time favored CLPN upon initial analysis while there was no difference in the overall complication rate, or in the severity or type of complications between the 2 groups. Significant improvements in WIT and EBL were noted in the RAPN group during the first 3 years of the learning curve with a plateau noted for WIT, EBL and operative time after the first 33 cases. Zero ischemia resections were avoided in the RAPN group early, likely affecting differences in WIT between the groups. After the RAPN learning curve was overcome outcomes appeared similar to those of the experienced laparoscopic surgeon who performed standard laparoscopic partial nephrectomy. Nephron sparing surgery for small renal masses is considered first line therapy according to the 2009 American Urological Association guidelines, although

SINGLE LAPAROSCOPIC SURGEON VERSUS MULTISURGEON ROBOT-ASSISTED NEPHRECTOMY

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Table 4. Pathological characteristics and outcomes of patients with positive surgical margins Pt No.

Nephrometry Score

Tumor Size (cm)

7A 8P 4X 9A 7P 4X

2.2 2.7 3.0 3.2 1.8 3.3

Clear cell Papillary Clear cell Clear cell Papillary Unclassified

5A 8A 6P 4P 9P

1.9 1.5 3.5 2.5 4.0

Chromophobe Chromophobe Clear cell Clear cell Clear cell

CLPN: 1 2 3 4 5 6 RAPN: 7 8 9 10 11

Final Pathology

partial nephrectomy remains underused while laparoscopic nephrectomy use is expanding.4,11,12 Laparoscopic partial nephrectomy is a technically difficult procedure with a reported complication rate as high as 30%.13 The robotic approach offers several advantages that may promote minimally invasive partial nephrectomy. Several comparisons between these approaches suggest an improved perioperative outcome for the robotic approach.14 A more recent, single surgeon, matched analysis showed similar outcomes for RAPN and CLPN.5 Our study differs from these comparisons in several ways. Our 2 cohorts were matched for nephrometry score, transabdominal vs retroperitoneal approach, Table 5. Pathological characteristics

Primary pathology: Benign Malignant Margin status: Pos Neg Furhman grade: 1 2 3 4 T stage: 1a 1b 2 3a 3b Secondary pathology: Clear cell Papillary Chromophobic Cystic Other

No. CLPN (%)

No. RAPN (%)

24 (22) 84 (78)

16 (15) 92 (85)

6 (7) 78 (93)

6 (7) 86 (93)

3 (4) 46 (58) 29 (37) 1 (1)

1 (1) 39 (48) 38 (48) 2 (3)

70 (83) 6 (7) 1 (1) 6 (7) 1 (1)

67 (73) 18 (20) 2 (2) 5 (5) 0

63 (75) 12 (14) 5 (6) 3 (4) 1 (1)*

56 (61) 17 (19) 12 (13) 3 (3) 4 (4)†

* Epitheloid angiomyolipoma. † Mucinous and unclassified renal cell carcinoma in 1 and 3 patients, respectively.

Fuhrman Grade

Final Stage

Management

Surveillance (mos)

3 2 4 2 2 3

T1aNxMx T3bNxMx T3aNxMx T1aNxMx T1aNxMx T3aNxMx

Surveillance Radical nephrectomy Cryoablation Surveillance Surveillance Surveillance

3 Not available Not available 8 34 19

n/a n/a 2 2 2

T1aNxMx T1aNxMx T1aNxMx T1aNxMx T1aNxMx

Surveillance Surveillance Surveillance Surveillance Surveillance

3 9 13 13 6

patient age and hilar tumor before statistical analysis to minimize the selection bias that may result from renal mass site or complexity, or patient comorbidity. Also, our comparison of an experienced laparoscopic surgeon to a heterogeneous group of early robotic surgeons makes our conclusions more generalizable to the population of surgeons who are currently adopting RAPN, in contrast to a single surgeon series. Perioperative outcomes, including EBL, WIT and operative time, were comparable to those of other studies in the literature.5,15 Complication rates in our series were somewhat higher than in the recently reported literature,3,16,17 although minor complications may be underreported. Our database was prospectively maintained with rigorous attention to tracking complications and deviations from the expected postoperative course, as intended by Dindo et al.10 This may account for the higher complication rate in our series. Most complications in each group were minor and intraoperative complications were rare. Also, most complications were nonurological, underscoring the importance of patient comorbidity in the perioperative outcome. The positive margin rate was higher in our series than in other reported series, including a recent study from our institution.13,18 Positive margins can be iatrogenic from tumor rupture during extirpation or artifact from cautery or trauma, or they may represent positive margins. Margin status was similar in the groups, although there were no positive margins in the RAPN group in the last year. Two patients in the CLPN group underwent further intervention to manage positive margins, including completion nephrectomy in 1 with no additional tumor identified on final pathological evaluation. It is unclear whether the higher positive margin rate in our series was due to differences in surgeon technique, tumor characteristics or pathological practices at our institution. The significance of positive surgical margins was been debated in recent studies.19,20

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SINGLE LAPAROSCOPIC SURGEON VERSUS MULTISURGEON ROBOT-ASSISTED NEPHRECTOMY

Although the positive margin rate is concerning, further close surveillance will be done to determine whether this compromises the oncological outcome. At our institution positive margins are often managed by observation after careful discussion of the risks and benefits with the patient. However, completion nephrectomy has been done in select circumstances. The limitations of our study deserve mention. Although our database is prospectively maintained, patients are not randomized, which introduces possible bias. We attempted to minimize this through matching. The difference in surgeon experience between CLPN and RAPN is notable. However, since it was impossible to adequately control for variable surgeon experience, we highlighted this difference in our comparison of these 2 minimally invasive approaches. Similar results for an experienced laparoscopic surgeon and for the initial experience of a large, heterogeneous group of robotic surgeons are encouraging. It indicates that the robotic approach may offer access to minimally invasive partial nephrectomy to more surgeons and patients. Also, several perioperative parameters in the RAPN group improved during the study period, indicating a reasonable learning curve for this approach.

With these limitations aside, we believe that our findings contribute to the growing literature evaluating the role of robotic assisted nephron sparing surgery. Our RAPN cohort is representative of a urological surgeon with previous laparoscopic experience in the early stages of adopting the robotic nephron sparing technique. The surgeon specific learning curve is difficult to assess, given the heterogeneity in the RAPN group. However, the institutional learning curve showing improved ischemia time, blood loss and operative time appeared to plateau after the first 33 cases in our series. The improvement in outcomes is likely explained by a combination of improvements in each individual surgeon as well as by increased familiarity with the procedure by the operative team.

CONCLUSIONS RAPN and CLPN have similar perioperative outcomes and complication rates when adjusting for tumor and patient factors, following a finite learning curve. Additional investigation is required to further define the benefit of this practice. The robotic platform may hasten the adoption of this technique and provide greater patient access to minimally invasive nephron sparing surgery.

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19. Lam JS, Bergman J, Breda A et al: Importance of surgical margins in the management of renal cell carcinoma. Nat Clin Pract Urol 2008; 5: 308. 20. Bensalah K, Pantuck AJ, Rioux-Leclercq N et al: Positive surgical margin appears to have negligible impact on survival of renal cell carcinomas treated by nephron-sparing surgery. Eur Urol 2010; 57: 466.