Laparoscopic Versus Open Radical Nephrectomy for Large Renal Tumors: A Long-Term Prospective Comparison A. K. Hemal,* A. Kumar, R. Kumar, P. Wadhwa, A. Seth and N. P. Gupta From the Department of Urology, All India Institute of Medical Sciences, New Delhi, India
Purpose: The role of laparoscopy in the management of large renal tumors (more than 7 cm) is not clearly established. We prospectively evaluated the feasibility, safety and long-term results of laparoscopic radical nephrectomy for large renal tumors (T2N0M0) and compared the results with those of open radical nephrectomy. Materials and Methods: Between 1998 and 2006, 112 patients with clinical stage T2N0M0 renal carcinoma underwent radical nephrectomy at our institution. Clinical data were prospectively collected after categorizing the patients into group 1— 41 with laparoscopy and group 2—71 with open surgery. The choice of procedure was nonrandomized and it depended on patient and surgeon preference and experience. Results: The 2 groups were contemporary and comparable in terms of age, body mass index and mean tumor size (9.9 and 10.1 cm, respectively). Concomitant adrenalectomy was performed in 14 patients (34%) in group 1 and in 29 (41%) in group 2. Limited (hilar) lymphadenectomy was performed in 30 patients (73%) in group 1 and in 58 (81%) in group 2. Group 1 patients experienced significantly less blood loss, and had a decreased analgesic requirement, shorter hospital stay and more rapid convalescence, although they required longer operative time (180.8 vs 165.3 minutes, p ⫽ 0.029). The 2 groups were followed for a similar period (mean 51.4 vs 57.2 months) and there was no difference in 5-year survival data. There were no local or port site recurrences. Conclusions: Laparoscopic radical nephrectomy for clinical stage T2 renal tumors is effective with the advantages of less blood loss, shorter hospital stay, decreased analgesic requirement and rapid recovery compared with open radical nephrectomy. Long-term results are also similar in the 2 groups of patients. Laparoscopic radical nephrectomy for large tumors is a technically difficult, challenging procedure and it should be attempted by surgeons with significant experience. Key Words: kidney, kidney neoplasms, laparoscopy, nephrectomy
pen radical nephrectomy is the mainstay of management for renal tumors.1 For tumors less than 7 cm (T1) laparoscopy has become a well established option with a number of groups reporting success equivalent to that of open surgery.2,3 In fact, LRN may even be considered the standard of care for such lesions in patients who are not candidates for nephron sparing surgery. Comparisons between laparoscopic and ORN have consistently demonstrated advantages in favor of the laparoscopic approach with regard to all perioperative morbidity indexes, including EBL, postoperative narcotic requirements, hospitalization and convalescence.3–7 Most of the current literature deals with laparoscopy for tumors less than 7 cm. The role of laparoscopy for large primary tumors (T2) is still under evaluation. To evaluate the feasibility, safety and long-term efficacy of laparoscopy in the management of these lesions we prospectively evaluated patients undergoing LRN for such tumors at our center and compared their data with those on a similar cohort of patients undergoing open surgery during the same period.
MATERIALS AND METHODS
O
Between 1998 and 2006 all patients undergoing radical nephrectomy for a clinical stage T2N0M0 renal tumor were included in this study. Tumor staging was based on standard imaging criteria and the procedure (laparoscopic vs open surgery) depended on the patient and surgeon choice. Only surgeons with significant laparoscopic experience performed laparoscopy, while all surgeons performed open surgery. LRN was performed using a standard transperitoneal or retroperitoneal route, as previously described.8 The retroperitoneal approach was used in 15 cases, while the remaining 26 were operated on using the transperitoneal approach. In a few patients dissection near the renal hilum was difficult because the renal mass prevented direct access to the renal vessels. In such cases after control of the gonadal vein the lower kidney pole was mobilized, followed by posterior dissection, which allowed the lower pole to be lifted up to dissect and control the renal vessels. While limited hilar lymph node dissection was performed in most patients, extended retroperitoneal lymph node dissection was not routinely performed. En bloc adrenalectomy was performed in patients with superior pole or large tumors. Specimen were removed intact without morcellation through a 5 to 7 cm incision by extending the port site incision after entrapment in a
Submitted for publication June 14, 2006. * Address for correspondence: Department of Urology, All India Institute of Medical Sciences, New Delhi-110 029, India (telephone: 91-11-26593249/2594884; FAX: 011-26588663/26588641; e-mail:
[email protected]).
0022-5347/07/1773-0862/0 THE JOURNAL OF UROLOGY® Copyright © 2007 by AMERICAN UROLOGICAL ASSOCIATION
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Vol. 177, 862-866, March 2007 Printed in U.S.A. DOI:10.1016/j.juro.2006.10.053
LAPAROSCOPIC VERSUS OPEN RADICAL NEPHRECTOMY FOR LARGE RENAL TUMORS commercial specimen entrapment device or a simple sterile plastic bag. Occasionally it was removed directly. Clinical data, including operative and postoperative management, and followup, were entered into a computerized database. Patients undergoing laparoscopy comprised group 1 and those undergoing open surgery comprised group 2. Followup in the 2 patient groups was similar, including clinical examination, kidney function tests, chest x-ray and ultrasonography or computerized tomography of the abdomen to detect port site, local or distant recurrence. Data on the 2 groups were compared statistically using the chisquare test for categorical variables, the Wilcoxon rank sum test for nonparametric variables and the Student t test for continuous variables. Kaplan-Meier analysis with log rank comparison was performed to estimate 5-year disease-free, cancer specific and overall survival.
RESULTS A total of 112 patients were included in the study period. This included 41 patients in group 1 (LRN) and 71 in group 2 (ORN). Patients in the 2 groups were comparable in age, sex, BMI and American Society of Anesthesiologists score. Mean tumor size was also comparable in the 2 groups of patients (table 1). Mean operative time was significantly greater in the laparoscopy group (table 1), although average EBL was significantly lower in this group despite similar specimen weights. Patients undergoing laparoscopy required less postoperative analgesics and they recovered more rapidly with shorter convalescence. In group 1 LRN was performed by the transperitoneal approach in 26 patients and through retroperitoneal access in 15. While transperitoneal procedures were successfully performed in all patients, retroperitoneal LRN was com-
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pleted in 13 with conversion to open surgery in 2. Concomitant adrenalectomy was performed in 14 patients (34%) in group 1 and in 29 (41%) in group 2. All adrenalectomy specimens were free of tumor involvement on histopathological evaluation. Limited (hilar) lymphadenectomy was performed in 30 patients (73%) in group 1 and in 58 (81%) in group 2. Two patients (4.9%) in group 1 and 7 (9.8%) in group 2 were found to have micrometastases in the lymph nodes at histological evaluation, thus, upgrading tumor stage in these patients. Two of the 4 intraoperative complications in group 1 necessitated conversion to open surgery (each retroperitoneal LRN), including 1 due to renal arterial bleeding secondary to clip dislodgment and the other due to bleeding from the renal vein. Bowel injury noted in group 1 was managed by intracorporeal suturing. Bowel injury (serosal tears) in 3 patients undergoing open surgery was also managed by primary repair. There was no statistical difference in the number of postoperative complications in the 2 groups but the open surgery group had a higher incidence of wound infection. The 2 patient groups were followed for a similar period (mean 51.4 vs 57.2 months). There were no local or port site recurrences. Table 2 shows the distant metastasis pattern. Two of the 3 patients with metastases in group 1 and 4 of the 7 with metastases in group 2 died of the disease. In addition, 3 patients in group 1 (stroke in 1 and myocardial infarction in 2) and 4 in group 2 (stroke in 1 and myocardial infarction in 3) died of noncancer related causes. Figures 1 and 2 show Kaplan-Meier curves for disease-free and overall survival, respectively. Five-year overall, diseasefree and cancer specific survival was similar in the 2 patient groups (table 2).
TABLE 1. Patient demographics, tumor characteristics, operative data and complications
Demographics ⫹ tumor characteristics: No. pts Mean ⫾ SD age (yrs) Mean ⫾ SD American Society of Anesthesiologists score Mean ⫾ SD BMI (kg/m2) No. men/women Mean ⫾ SD tumor size (cm) % Rt tumor Intraoperative and perioperative data: Mean ⫾ SD operative time (mins) Mean ⫾ SD EBL (ml) No. blood transfusion (%) No. conversion to open (%) Mean ⫾ SD specimen weight (gm) Mean ⫾ SD analgesic requirement (mg morphine equivalent) Mean ⫾ SD hospital stay (days) Mean ⫾ SD convalescence (wks) No. RCC (%) No. oncocytoma (%) No. complications: Intraop vascular/hemorrhage Intraop bowel Intraop totals Postop wound infection Postop delayed bleeding Postop atelectasis Postop ileus Postop incisional hernia Postop totals
Group 1
Group 2
p Value
41 52.5 ⫾ 11.3 1.95 ⫾ 0.95 29.4 ⫾ 4.5 24/17 9.9 ⫾ 2.2 46.3
71 52.7 ⫾ 11.8 1.75 ⫾ 0.75 29 ⫾ 3.4 47/24 10.1 ⫾ 3.2 59.1
0.94 0.23 0.62 0.418 0.69 0.19
180.8 ⫾ 21.5 245.5 ⫾ 125.13 6 (14.63) 2 (4.87) 725 ⫾ 234 16.4 ⫾ 3.35 3.6 ⫾ 0.79 1.56 ⫾ 0.5 39 (95.1) 2 (4.9)
165.3 ⫾ 40.9 537.3 ⫾ 139.99 23 (32.4) Not applicable 795 ⫾ 281 35.0 ⫾ 8.01 6.6 ⫾ 1.06 3.3 ⫾ 0.69 68 (95.7) 3 (4.3)
0.029 (significant) ⬍0.001 (significant) 0.04 (significant) 0.18 ⬍0.001 (significant) ⬍0.001 (significant) ⬍0.001 (significant) 0.75
3 1
5 3
4 (9.75%) 1 2 1 1 0
8 (11.26%) 5 2 1 2 1
0.94
5 (12.19%)
11 (15.49%)
0.84
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LAPAROSCOPIC VERSUS OPEN RADICAL NEPHRECTOMY FOR LARGE RENAL TUMORS TABLE 2. Followup data
No. pts Mean mos followup (range) No. distant metastases (%) No. metastasis sites: Lung Brain Skeleton % 5-Yr survival: Overall Ca specific Recurrence-free
Group 1
Group 2
p Value
41 51.4 (3–78) 3 (7.3)
71 57.2 (4–80) 7 (9.85)
0.20 0.91
2 1 87.8 95.12 92.6
4 1 2 88.7 94.36 90.1
0.87 0.79 0.91
No local recurrences and no significant p values.
DISCUSSION LRN has emerged as the standard of care in most patients with T1 renal tumors who are not candidates for nephron sparing surgery.2,3,6 Even in the early years of the learning curve initial published series consistently revealed that laparoscopic nephrectomy was not only immediately as effective as open surgical extirpation, but also significantly better tolerated than open surgery.9 –11 Laparoscopy resulted in outcomes similar to those of open surgery with no local or port site recurrences and an equivalent incidence of metastases. While most series are confined to small stage T1 tumors, a few recent publications addressed the role of LRN for large renal tumors.4,6,12,13 Changes in the outcomes of larger tumor management allowed even primary tumors greater than 4 cm to be included in the T1 category and the focus of evaluation of laparoscopy as a modality for management shifted to tumors greater than 7 cm, which now forms the T2 category of primary tumors.14 As specimen size increases, several unique technical problems arise during laparoscopic surgery. They include a decreased working space, maintenance of operator orientation, increased potential for adjacent organ involvement, significant parasitic vessels and difficult specimen removal.12 We have significant experience with retroperitoneoscopic nephrectomy and it is our preferred access for managing
FIG. 1. Kaplan-Meier recurrence-free survival curve
FIG. 2. Kaplan-Meier overall survival curve
benign nonfunctioning kidneys.15 We also perform retroperitoneoscopic radical nephrectomy for T1 tumors. However, larger T2 tumors presented a comparatively limited working space, making the procedure more cumbersome. Thus, in our experience transperitoneal access seems to be the preferred route for dealing with such large tumors. After nephrectomy intact specimen extraction is preferable to allow full pathological assessment. This can be best accomplished using a laparoscopic specimen entrapment device with removal through a muscle splitting, flank, lower abdominal modified Gibson or Pfannenstiel incision.12 In our series the specimen was extracted through a flank incision by extending or connecting port sites using a commercial entrapment device or simple plastic bag. It is not important to use a high quality, impermeable bag because morcellation is not performed and they are simply being used to remove the specimen from the body. HAL for radical nephrectomy has been used as a bridging technique for the novice laparoscopist, while others extol the virtues of the tactile control and improved comfort level of the procedure as well as eventual use of the hand port for extracting the specimen. Alternatively from the purely laparoscopist view it entails the use of a cumbersome device that encroaches on the working space, causes hand discomfort and adds to the cost of the procedure. Patel and Leveillee observed the requirement of an equivalent operative time for HAL radical nephrectomy for 50 T1 and 10 T2 tumors with little blood loss and complication rates.16 They emphasized the need for adequate experience before treating larger tumors. Malaeb et al found HAL radical nephrectomy to be technically feasible and advantageous for T2 tumors over ORN (mean size 9.7 vs 12.3 cm), although tumors greater than 15 cm necessitated ORN.17 Our data demonstrate that, compared with ORN in a contemporary cohort of patients, LRN for large T2 tumors results in similar rates of intraoperative and postoperative complications. There was certainly an increase in operative time but some of this could have been due to our
LAPAROSCOPIC VERSUS OPEN RADICAL NEPHRECTOMY FOR LARGE RENAL TUMORS learning curve since this series includes all of our cases, including the initial ones. Moreover, increased operative time did not result in any adverse patient outcome and it may also not have been significant economically since it resulted in less hospitalization and convalescence time. When treating a large tumor, it is prudent to be careful and steady during the surgery since large parasitic vessels and an exophytic component of the tumor in the anteromedial aspect of the kidney makes the dissection of renal vessels difficult with an increased risk of transgressing oncological principles or causing major vascular injury. The advantages that we found in our laparoscopy patients are similar to those that have been proved in patients undergoing this surgery for smaller tumors. When comparing a similar group of patients undergoing laparoscopy or open surgery, Dunn et al noted the advantages that laparoscopy offered in terms of analgesic requirement, hospital stay, blood loss, ambulation and return to normal activity.4 This advantage was found to persist for larger tumors with no additional complications when performed by a group of expert laparoscopists.13 One of the important parameters of long-term efficacy of oncological surgery is local recurrence since a higher rate may indicate less than complete tumor removal. A specific concern with laparoscopy is the possibility of port site recurrence. None of the patients in our series had either of these complications and 5-year survival in the 2 groups was similar. Our results are similar to those reported by others for stage T2 tumors.6,18,19 The role of formal lymphadenectomy for RCC in the absence of clinically evident nodes is still much debated, although it has a role in prognosticating and staging the disease. Limited lymphadenectomy allows an equal opportunity in providing similar information. Arguably a small subset of patients may benefit from extended lymphadenectomy, translating as an improved survival benefit. However, a review of cases of RCC undergoing retroperitoneal lymphadenectomy in an 11-year period was unable to demonstrate any survival benefit or improved staging information in patients with clinically node negative disease at followup.20 We believe that our success with such large tumors significantly depends on our experience with advanced laparoscopy. This allowed better instrument control and orientation, and a higher threshold for conversion to open surgery. It is significant that most of the current literature on laparoscopy for large tumors also comes from centers with a well established laparoscopy team. On rare occasions preoperative angio-infarction of a large tumor may facilitate the performance of LRN. However, this was not required in any of our patients.
ing spontaneous modifications of surgical steps to ensure a safe outcome. Advanced surgical skills are required before it is attempted.
Abbreviations and Acronyms BMI EBL HAL LRN ORN RCC
⫽ ⫽ ⫽ ⫽ ⫽ ⫽
body mass index estimated blood loss hand assisted laparoscopy laparoscopic radical nephrectomy open radical nephrectomy renal cell carcinoma
REFERENCES 1. 2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12. 13.
CONCLUSIONS LRN is as safe as open surgery for large renal tumors, whether done by a transperitoneal or a retroperitoneal approach. Immediate and long-term outcomes of the 2 procedures are similar with patients undergoing LRN having the benefit of less blood loss, analgesic requirement, hospitalization and convalescence. However, LRN for large renal tumors is a difficult operation, often requir-
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14. 15.
16.
Robson CJ: Radical nephrectomy for renal cell carcinoma. J Urol 1963; 89: 37. Ono Y, Kinukawa T, Hattori R, Gotoh M, Kamihira O and Ohshima S: The long-term outcome of laparoscopic radical nephrectomy for small renal cell carcinoma. J Urol 2001; 165: 1867. Gill IS, Meraney AM, Schweizer DK, Savage SS, Hobart MG, Sung GT et al: Laparoscopic radical nephrectomy in 100 patients: a single center experience from the United States. Cancer 2001; 92: 1843. Dunn MD, Portis AJ, Shalhav AL, Elbahnasy AM, Heidorn C, McDougall EM et al: Laparoscopic versus open radical nephrectomy: a 9-year experience. J Urol 2000; 164: 1153. Gill IS, Schweizer D, Hobart MG, Sung GT, Klein EA and Novick AC: Retroperitoneal laparoscopic radical nephrectomy: the Cleveland Clinic experience. J Urol 2000; 163: 1665. Portis AJ, Yan Y, Landman J, Chen C, Barrett PH and Fentie DD: Long-term follow up after laparoscopic radical nephrectomy. J Urol 2002; 167: 1257. Pautler SE, Richards C, Libutti SK, Linehan WM and Walther MM: Intentional resection of the diaphragm during cytoreductive laparoscopic radical nephrectomy. J Urol 2002; 167: 48. Goel A, Hemal AK and Gupta NP: Retroperitoneal laparoscopic radical nephrectomy and nephroureterectomy and comparison with open surgery. World J Urol 2002; 20: 219. Kavoussi LR, Kerbl K, Capelouto CC, McDougall EM and Clayman RV: Laparoscopic radical nephrectomy for renal neoplasms. Urology 1993; 42: 603. McDougall E, Clayman RV and Elashry OM: Laparoscopic radical nephrectomy for renal tumor: the Washington University experience. J Urol 1996; 155: 1180. Cadeddu JA, Ono Y, Clayman RV, Barrett PH, Janetschek G, Fentie DD et al: Laparoscopic nephrectomy for renal cell cancer: evaluation of efficacy and safety: a multicenter experience. Urology 1998; 52: 773. Fenn NJ and Gill IS: The expanding indications for laparoscopic radical nephrectomy. BJU Int 2004; 94: 761. Steinberg AP, Finelli A, Desai MM, Abreu SC, Ramani AP, Spaliviero M et al: Laparoscopic radical nephrectomy for large (greater than 7 cm, T2) renal tumors. J Urol 2004; 172: 2172. Sobin LH and Wittekind C: TNM Classification of Malignant Tumors, 6th ed. New Jersey: Wiley 2002. Hemal AK, Gupta NP and Kumar R: Comparison between retroperitoneoscopic nephrectomy and open surgery for tubercular non-functioning kidneys. J Urol 2000; 164: 32. Patel VR and Leveillee RJ: Hand-assisted laparoscopic nephrectomy for stage T1 and large stage T2 renal tumors. J Endourol 2003; 17: 379.
866 17.
LAPAROSCOPIC VERSUS OPEN RADICAL NEPHRECTOMY FOR LARGE RENAL TUMORS
Malaeb BS, Sherwood JB, Taylor GD, Duchene DA, Broder KJ and Koeneman KS: Hand-assisted laparoscopic nephrectomy for renal masses ⬎9.5 cm: series comparison with open radical nephrectomy. Urol Oncol 2005; 23: 323. 18. Chan D, Cadeddu JA, Jarett TW, Marshall FF and Kavoussi LR: Laparoscopic radical nephrectomy: cancer control for renal cell carcinoma. J Urol 2001; 166: 1109.
19.
Permpongkosol S, Chan DY, Link RE, Sroka M, Allaf M and Kavoussi LR: Long-term survival analysis after laparoscopic radical nephrectomy. J Urol 2005; 174: 1222. 20. Pantuck AJ, Zisman A, Dorey F, Chao DH, Han KR, Said J et al: Renal cell carcinoma with retroperitoneal lymph nodes. Role of lymph node dissection. J Urol 2003; 169: 2076.
