- Email: [email protected]
Laparoscopic Radical Nephrectomy: The Nagoya Experience
\'id 1.58. 719-723. September 1997
Prrrircrl
in
1I.S.A.
LAPAROSCOPIC RADICAL NEPHRECTOMY: THE NAGOYA EXPERIENCE YOSHINARI ONO, NORIO KATOH, TSUNEO KINUKAWA, OSAMU MATSUURA SHINICHI OHSHIMA
AND
Fro111 the Department of Urology, Komaki Shitrim Hospital, Okazaki City Hospital, and Shakar Hokeri C h u k w Hospital, Kornaki shi, Japan
ABSTRACT
Purpose: We evaluated the efficacy of laparoscopic radical nephrectomy for removing kidneys with small volume renal cell carcinoma. Materials and Methods: 25 patients (19 men and 6 women, mean age 59) who had a kidney with small volume renal cell carcinoma (diameter less than 5 cm.), underwent laparoscopic radical nephrectomy. The kidney was dissected laparoscopically together with the adrenal gland, perirenal fatty tissue and Gerota's fascia. In 11 patients, we used the transperitoneal approach and in the remaining 14 we used the retroperitoneal approach, in which a working space is created by finger and balloon dissection. We maneuvered the kidney into the laparoscopy sack, which was then removed through an additional 5 to 6 cm. incision. Results: All 25 kidneys were removed successfully. Mean operation time was 5.3 hours and mean estimated blood loss was 335 ml. There were 5 complications, including a patient who suffered an injury to the duodenum, which was treated by open duodenojejunostomy. Full convalescence occurred a t an average 23 days. No metastatic disease, no local recurrence and no seeding a t the port sites occurred during the followup of 7 to 49 months (mean, 22 months). Conclusions: Laparoscopic radical nephrectomy is recommended a s a minimally invasive procedure for removing kidneys with small volume renal cell carcinoma. KEYWORDS:carcinoma, renal cell, nephrectomy, laparoscopy
Laparoscopic nephrectomy has been performed to remove kidneys with various benign and malignant diseases since the first clinical success by Clayman e t al in July 1990.1-1" Although i t has been accepted as a minimally invasive procedure for removing kidneys with benign diseases, it is still controversial as a procedure for removing kidneys with malignant diseases. We started a laparoscopic nephrectomy program for benign renal diseases in July 1991.4 So far, 50 of 54 patients with severely damaged kidneys have been treated successfully.i.14 We started a laparoscopic radical nephrectomy program for malignant renal diseases in July 1992.' Under laparoscopic observation, we ligate the renal vessels and then dissect the kidney together with the adrenal gland, perirenal fatty tissue and Gerota's fascia. So far, 25 patients with small volume renal cell carcinomas have been treated. We present our procedure for laparoscopic radical nephrectomy and the clinical results for our 25 patients. MATERIALS A N D METHODS
Since July 1992, we have performed laparoscopic radical nephrectomy on 25 patients with small volume renal cell carcinomas of less than 5 cm. in diameter (see table). Initially, we used t h e previously described transperitoneal approach;2,7," our first 11 patients were treated in that way. Then, in September 1994, we developed the retroperitoneal approach; our next 14 patients were treated in this way. Between July 1992 and December 1995, we performed open radical nephrectomy on 17 patients with low stage renal cell carcinomas at our hospitals. We compared all data, including information on long-term recovery, that we obtained from our 2 groups of patients. Preoperative preparation. All 25 patients underwent bowel preparation as described previously.',7 I n t h e first 2 1 cases, the renal arteries were embolized the day before or the day of Accepted for publication January 10,1997.
surgery to minimize blood loss and to manage the great renal vessels more easily and quickly during surgery. This practice was abandoned in January 1996 because renal arterial embolization is invasive, and we had learned to manage the great renal vessels efficiently. After the induction of general anesthesia, patients who were undergoing a transperitoneal procedure were placed in a semilateral (70-degree)position, and patients undergoing a retroperitoneal procedure were placed in a lateral position. Radical nephrertomy via the transperitoneal approach. Operative procedures were described previously.'. After duodenum injury occurred because of the use of a 5 mm. Padron'* retractor, however, we have placed a 12 mm. trocar instead in the midclavicular line 5 to 6 cm. above the level of the umbilicus so t h a t we can now use a safer 10-mm. Padron retractor. Radical nephrectomy uia the retroperitoneal approach. A 3 cm. incision was made along t h e anterior axillary line 1 cm. below t h e level of the umbilicus. The external and internal oblique muscles and the transversus abdominalis were divided bluntly with retractors. The exposed Gerota's fascia was dissected digitally from the quadrant lumbotum and psoas muscle. A balloon, consisting of the middle finger of a size 8 surgeon's glove tied to t h e top of a rigid nephroscope, was placed behind the kidney and, under direct vision through the rigid nephroscope, was inflated with 1,000 ml. of normal saline to produce a working space. This inflation was maintained for 5 minutes to allow hemostasis to take place (fig. 1).After the peritoneum was digitally dissected medially from the abdominal wall, a 12 mm. trocar was inserted 5 to 6 cm. above the first incision (fig.2, B ) under digital control as described previously.'.' In the posterior axillary line, a 12 mm. trocar was placed at the level of the umbilicus (fig. 2, C ) and a 5 mm. trocar 5 to 6 cm. above the level of the umbilicus (fig. 2, D).In the midaxillary line, a 12 mm. trocar was placed
719
* damner Surgical Instruments Inc., Hawthorne,
New York.
720
LAPAROSCOPIC RADICAL NEPHRECTOMY Patients’ characteristics and results
.n. .
No.--AgeSex
Side
Owrative Time thrs.1
14 2 -52 3 -56 4 -51 5 -72 6 4 7 -50 8 -52 9 -52 10 4 1 11 4 3
-M -hi
Rt. Lt. Lt. Rt. Rt. Rt. Lt . Rt. Rt. Rt. Lt.
6.3 7.7 6.5 5.1 6.3 5.0 6.5 4.2 5.2 6.8 6.0
450 800 100 400 400 200 900 400 190 132 395
12 -74
-M
Rt. Rt. Rt . Rt. Rt. Lt. Lt. Rt. Rt. Rt . Rt . Rt . Lt. Lt.
3.7 3.9 5.2 5.5 5.3 4.0 3.0 6.4 4.8 6.9 4.3 4.1 5.0 5.9
100 50 100 290 279 700 145 480 96 386 160 50 618 552
-F -M
-M -M
-M -F -M
-M -M
13 4 8 -F
14 4 4 15 - 4 8 16 4 9 17 -70 18 -59 19 -56 20 -57 21 -48 22 -74 23 - 4 7 24 -77 25 4 8
-M -M
-M -F -F -M -M -M -F
-M -M -M
Estimated Blood Loss (rnl.1
Removal
Success Success Success Success Success Success Success Success Success Success Success
~
Complication
Tronspentoneal approach No Injury of spleen No No No No Injury of adrenal gland No Injury of duodenum No No Retroperitoneol approach Success No Success No Success No Success No Success No Success Bleeding from penureteric artery No Success Success No Success No Success No Success No Success No Success No
Success
Paralytic ileus
-
Pathological Findings i stage/gradel
Wt.
Renal cell Ca tpTlpNOG2l Renal cell Ca cpT2pNOGlI Renal cell Ca (pTlpNOC21 Renal cell Ca (pTlpNOG1) Renal cell Ca tpTLpNOG21 Renal cell Ca tpT2pNOC.2) Renal cell Ca tpT2pNOC.21 Renal cell Ca IpTLZpNOGlI Renal cell Ca (pT2pNOG21 Renal cell Ca ipT2pNOG21 Renal cell Ca tpT2pNOG2I
310 500 165 330 160 270 340 220 426 360 346
Renal cell Ca (pTlpNOG11 Renal cell Ca cpTZpN0G21 Renal cell Ca (pTlpNOG1 I Renal cell Ca (pTlpNOG21 Renal cell Ca (pT3pNOG2 I Renal cell Ca (pT2bpNOG21 Renal cell Ca (pT2pNOG2 I Renal cell Ca (pT2pNOG21 Renal cell Ca (pT2pNOG2) Renal cell Ca tpT2pNOG21 Renal cell Ca tpT2pNOGlI Renal cell Ca 1pT2pNOG21 Renal cell Ca (pT2pNOG21 Renal cell Ca loT3oNOG2 I
215 170 330 420 176 210 162 490 255 368 230 322 190 250
FIG. 1. Balloon dissection in retroperitoneal space. Balloon is inflated with 1,000 ml. of saline to produce working space in posterior aspect of kidney.
at the level of the umbilicus (fig. 2, E ) . A 12 mm. Origin* trocar was placed in the site of the first incision (fig. 2, A), which was sutured to prevent carbon dioxide leakage. Carbon dioxide insumation at a pressure of 12 mm. Hg maintained the working space in the retroperitoneal cavity. A 0-degree laparoscope was inserted through port A for observation, and a 10 mm. retractor was introduced through port B to deflect the peritoneum medially. The procedure for dissecting the kidney was basically the same as in the transperitoneal approach. The ureter was identified, exposed and dissected before being secured with ligature clips and transected with scissors. After retracting the kidney medially, the lateral wall of the vena cava or the aorta was dissected and exposed upward. Then the renal vessels were exposed and dissected. In cases of disease on the * Origin Medsystems Inc., Menlo Park, CA.
right side, the renal artery was secured with ligature clips before being transected with scissors and the adrenal arteries were divided by electrocautery. In cases of disease on the left side, the renal vein was secured and transected proximally to the left adrenal vein and the left gonadal vein by endoscopic gastrointestinal anastomosis vascular stapler, and the adrenal arteries were divided by electrocautery. In the anterior aspect of the kidney, the anterior lobe of Gerota’s fascia was dissected from the peritoneum. As we retracted the kidney downward, the right adrenal gland was dissected out from the liver, the diaphragm and the psoas muscle, and the left adrenal gland from the tail of the pancreas, the diaphragm and the psoas muscle. The double-layered laparoscopy sack of impermeable plastic and nondistensible nylon was equipped with a plasticcoated guide wire through its top that allowed us to open and
LAPAROSCOPIC RADICAL NEPHRECTOMY
721
ng the ureter. Hemostasis was achieved laparoscopically in :hese 3 cases, with 2 patients (cases 7 and 17) each requiring transfusion of 2 units of blood. Duodenal perforation was iiscovered in 1 patient on the day after surgery on the right side (case 9), when bile was discharged from the drainage tube. The injury might have been caused by a 5 mm. Padron endoscopic exposing retractor, although it had not been no/I I ticed during the laparoscopic surgery. The patient was treated successfully with open duodenojejunostomy. Three of the complications (cases 2, 7, 9) occurred during the transperitoneal procedure and 1 (case 17) during the retroperitoneal procedure. In 21 cases, the kidney could be entrapped in the laparosPosterior Anterior copy sack, but 4 kidneys (cases 9, 12, 16, 23) could not. In 1 Axillary Axillary patient, who was treated transperitoneally (case 9). the Line Line weight of the dissected mass was 426 gm. In the other 3 Line Line patients, who were treated retroperitoneally (cases 12, 16, FIG.2. Location of ports in transperitoneal (Zefl) and retroperito- 23), the weights of the dissected masses were 215, 176 and neal (right) radical nephrectomy. 322 gm., respectively. However, in these cases, the working space was too small to entrap the kidneys. The 4 kidneys close it firmly.14.16.17Trocar A was removed and the sack was were removed by hand through the enlarged first incision, introduced into the working space through this first incision, which in 2 cases was further enlarged by about 2 cm. and which was then closed again. After renewed carbon dioxide kept open with retractors. Operative time was between 3 and 7.7 hours (mean 5.3 insufflation, the specimen that included the kidney, the adrenal gland, perirenal fatty tissue and Gerota's fascia was hours); in the transperitoneal approach it was between 4.2 maneuvered together into the sack under laparoscopic obser- and 7.7 hours (mean, 6 hours) and in the retroperitoneal vation without being morseled or minced. The sack was approach it was between 3 and 6.9 hours (mean, 4.9 hours). pulled out through the first incision, which was enlarged Overall estimated blood loss was between 50 and 900 ml. vertically toward port B by an additional 5 to 6 cm. skin and (mean 335 ml.); in the transperitoneal approach, it was bemuscle incision in the transperitoneal approach, and an ad- tween 100 and 900 ml. (mean 397 ml.), and in the retroperditional 5 to 6 cm. skin incision and blunt abdominal muscle itoneal approach, it was between 50 and 700 ml. (mean 285 division in the retroperitoneal approach. The incision was m1.h Postoperatively, an average of 43 mg. of pentazocine closed by 2 layers of interrupted muscle suture and inter- w a s given intramuscularly to 20 patients and the remaining rupted skin suture. As the 4 other trocars were removed, a 5 patients did not request analgesics. There was only 1 comPenrose* drain was routinely placed through port E in the plication in the early postoperative period. One patient (case renal bed to determine postoperative blood loss. The drainage 25) had paralytic ileus, which was successfully treated by tube was removed 1 or 2 days later as described previ~usly.~ conservative therapy. Postoperative hospital stay was between 7 and 17 days (mean l l days), and full convalescence occurred between days 16 and 46 (mean day 23). These figRESULTS ures exclude the patient (case 9) who underwent duodenojeThe 11 patients (9 men and 2 women) who underwent jenostomy, stayed in the hospital for 30 days after the surtransperitoneal laparoscopic radical nephrectomy were be- gery, and achieved full convalescence on day 45. There were tween 44 and 83 years old (mean age 57). Seven patients had no differences in the administration of analgesics, hospital disease on the right side and 4 had disease on the left side. stay and the period to full convalescence between the paThe preoperative diagnosis was TlNOMO disease in 3 pa- tients treated transperitoneally and those treated retroperitients and T2NOMO disease in 8 patients. No patient had toneally. undergone abdominal surgery. All 25 specimens were removed intact without being morThe 14 patients (10 men and 4 women) who underwent seled or minced. Their weight was between 162 and 500 gm. retroperitoneal laparoscopic radical nephrectomy were be- (mean 289 gm.), and the tumor size was between 20 X 20 x tween 48 and 77 years old (mean age 60). Ten patients had 20 mm. and 50 x 40 x 40 mm. The number of removed lymph disease on the right side and 4 patients had disease on the nodes was between 1 and 10 (mean 4). none of which had left side. The preoperative diagnosis was TlNOMO disease in metastasis. Final pathological analysis revealed that the re2 patients and T2NOMO disease in 12 patients. Four patients nal cell carcinoma was stage pT1 in 6, pT2 in 17, and pT3a in had undergone abdominal surgery; one patient (case 16) with 2 patients. The followup period was between 7 and 49 months an affected right native kidney had received a renal trans- (mean 22), and no patient had a metastatic disease, a local plant, and the other 3 patients had had open transperitoneal recurrence or seeding at the port sites. hysterectomy (case 18), open colectomy (case 20) and open The 17 patients (12 men and 5 women) who underwent radical prostatectomy (case 24). Statistical analysis was per- open radical nephrectomy were between 44 and 80 years old formed with Student's t test. (mean age 61).Ten patients had disease on the right side and All 25 kidneys were dissected successfully and completely 7 had disease on the left side. Two patients had pTlpNOpMO through either the transperitoneal or the retroperitoneal ap- disease and 15 had pT2pNOpMO disease. The weights of the proach. Of the 14 retroperitoneal cases that included 4 pa- specimens were between 300 and 504 gm. (mean 375 gm.). tients with previous abdominal surgery, balloon dissection Operative time was between 3 and 5.6 hours (mean 3.6), successfully created a working space without causing any which was shorter than in the laparoscopically treated group bleeding. It took 0.4 to 0.7 hours (mean 0.6 hours) to create (p <0.001). Blood loss was between 141 and 844 ml. (mean the retroperitoneal working space. 474). There was no significant difference between the 2 There were 4 intraoperative complications: bleeding from groups. Postoperatively, a n average of 63 mg. pentazocine an injured spleen (case 2) and an injured adrenal gland (case was given intramuscularly to all 17 patients, which was a 7),both caused by improper retraction, and bleeding from a n larger dose than in the group treated laparoscopically (p injured periureteral artery (case 17) caused by the clip secur- <0.01). There were 2 complications. Two patients had paralytic ileus, which could successfully be treated by conserva* Fuji Systems Co., Tokyo, Japan.
I
I
I
\
I
722
LAPAROSCOPIC RADICAL NEPHRECTOMY
tive therapy. Postoperative hospital stay was between 15 and 35 days (mean 24), which was significantly longer than in the group treated laparoscopically ( p <0.001). Full convalescence occurred between days 42 and 90 (mean day 64), which was also significantly longer than in the group treated laparoscopically ip < 0 . 0 0 1 ~ I~lscrssIo~ Radical nephrectomy has been the standard treatment for localized renal cell carcinoma since the initial report by Robson in 1963.'* The procedure includes ligation of the renal vessels before manipulation of the tumor, removal of the kidney and adrenal gland together with the perirenal fatty tissue and Gerota's fascia, and lymph node dissection. We first performed radical nephrectomy as a laparoscopic procedure in July 1992,2 when we removed a kidney with a small volume renal cell carcinoma. A total of 25 patients with a renal cell carcinoma of less t h a n 5 cm. in diameter has been treated in this manner. In our laparoscopic procedures, ligation of the renal vessels is accomplished by early identification of the ureter and cephalad dissection along the great vessels without manipulation of the tumor. The removal of the kidney and adrenal gland together with the penrenal fatty tissue and Gerota's fascia is also accomplished without technical difficulty. However, laparoscopic lymph node dissection cannot be performed at present and it is particularly difficult in cases with disease on the right side. This is why we choose laparoscopic radical nephrectomy only for cases of small volume renal cell carcinoma, which do not normally have microscopic lymph node involvement. I n our series, mean operative time was 5.3 hours, mean estimated blood loss was 335 ml., and there were 4 intraoperative and 1 postoperative complications. These results are not as good as those of the open procedure. Three of the 4 intraoperative complications occurred in the first group of patients who were treated transperitoneally. They were caused by improper retraction of intra-abdominal organs. After the duodenum injury occurred, we used a 10 mm. instead of a 5 mm. Padron retractor, which reduces the risk of injury to intra-abdominal organs such as the duodenum and spleen. Learning curve effects have helped us improve our operative techniques. McDougall et al described several postoperative complications, such as heart failure and wound hernia, which, fortunately, we did not see in our patients.I3 Although 1 patient was hospitalized longer with a complication, the other 24 patients treated by laparoscopic surgery recovered faster and returned to their normal activities earlier than the 17 patients treated by open surgery. No metastatic disease, no local recurrence and no port site seeding was found in 7 to 49 months of followup (mean 22). These data suggest that laparoscopic radical nephrectomy is a minimally invasive procedure to be recommended for removing kidneys with small volume renal cell carcinoma. As with laparoscopic simple nephrectomy, laparoscopic radical nephrectomy was first performed via the transperitoneal approach. In our series, the first 11 patients were treated transperitoneally. The problems we encountered, such as injury to intra-abdominal organs and the difficulty of retracting them, are inherent to the transperitoneal approach. We therefore applied the retroperitoneal approach to laparoscopic radical nephrectomy. Between September 1994 and January 1996, the next 14 patients were treated retroperitoneally. We encountered only 1 problem, an injury to the periureteral artery. We also successfully removed kidneys from patients with a history of abdominal surgery. We modified Gaur's original retroperitoneal method. 1.1 We made the first 3 cm. incision in the anterior axillary line 1 cm. below the level of the umbilicus, which greatly facilitates the establishment of the ports in the anterior axillary line. We used a balloon tied to the top of a rigid nephroscope for
dissection when creating the retroperitoneal working space, because the position of the balloon can be controlled easily and because the progress of dissection can be monitored under direct vision. We performed finger and balloon dissection only in the posterior aspect of the kidney, however, because this technique does not allow the exact dissection of the Gerota's fascia from t h e peritoneum and poses the threat of injury to both; we used laparoscopic forceps instead. As have other groups,1o we encountered injuries to abdominal organs in our transperitoneal approach. I n contrast, we encountered no injuries to abdominal organs in our retroperitoneal approach. There is obviously less risk of injury to abdominal organs when all manipulations are restricted to the retroperitoneal space. Our retroperitoneal procedures had a shorter mean operating time than the transperitoneal procedures we or other groups performed.11-'4 Creating a working space in the retroperitoneal cavity was time-consuming but subsequently allowed easy dissection of the ureter and renal vessels. The retroperitoneal approach also makes some transperitoneal maneuvers redundant, such as the incision of the peritoneum and the dissection of the posterior aspect of the kidney. Lesser risk of injury to abdominal organs and shorter OPerative time seem to be advantages of the retroperitoneal approach. However, our series was not a randomized study and the retroperitoneally treated patients have benefited from our learning curve. Thus we must not draw final conclusions about the efficacy of the retroperitoneal approach in laparoscopic radical nephrectomy. The working space created retroperitoneally is smaller than the one available transperitoneally, which makes the entrapment of the renal specimen more difficult even in simple n e p h r e ~ t o m y .14~ ~I.n our 14 retroperitoneal radical nephrectomies, we encountered 3 cases in which the successfully dissected mass could not be reduced in size and could not be entrapped in the sack because the working space was too small. We had to enlarge the original incision, which erased the greatest advantage of laparoscopic radical nephrectomy, that is its minimally invasive nature. The small working space could be the critical disadvantage of the retroperitoneal approach in laparoscopic radical nephrectomy. Large kidneys should therefore be removed by transperitoneal laparoscopic radical nephrectomy or by the combined method of McDougall et al, who open t h e peritoneum to obtain a sufficiently large working space after dissection of the kidney through the retroperitoneal approach. 1:' Our current work focuses on t h e advantages and disadvantages of morseling and mincing the dissected mass as means of preserving minimal invasiveness. CONCLUSIONS
Our results support previous reports", t h a t recommend laparoscopic radical nephrectomy for removing kidneys with small volume renal cell carcinomas. However, it is necessary to gather more long-term data on patients to determine whether laparoscopy is superior to open surgery in radical nephrectomy. The retroperitoneal approach should be selected when the patient has a history of abdominal surgery or when the condition indicates that a shorter operating time is important. REFERENCES
1. Clayman, R. V., Kavoussi, L. R., Soper, N. J., Dierks, S. M., Meretyk, S., Darcy, M. D., Roemer, F. D., Pingleton, E. D., Thomson, P. G . and Long, S. R.: Laparoscopic nephrectomy: Initial case report. J. Urol., 146: 278, 1991. 2. Ono, Y., Sahashi, M., Yamada, S. and Ohshima. S.: Laparoscopic nephrectomy without morcellation for renal cell carcinoma: Report of initial 2 cases. J. Urol., 1 5 0 1222, 1993. 3. Terachi. T.. Matsuda, T., Kawakita. M., Mikami. O., Hoiii, Y.,
LAPAROSCOPIC RADICAL NEPHRECTOMY Ogura, K., Takeuchi, H., Komatsu, Y. and Yoshida, 0.:Laparoscopic nephrectomy: A report of 13 cases. Jap. J. Endourol. ESWL, 6: 133, 1993. 4. Katoh, N., Ono, Y., Yamada, S., Kinukawa, T., Sahashi, M., Matsuura, M., Hirabayashi, S., Hatano, Y., Sakakibara, T. and Ohshima, S.: Review of laparoscopic nephrectomy in 26 patients. J a p . J. Endourol. ESWL, 6 129, 1993. 5. Kavoussi, L. R., Kerbl, K., Capelouto, C. C., McDougall, E. M. and Clayman, R. V.: Laparoscopic nephrectomy for renal neoplasms. Urology, 42: 603, 1993. 6 . Kerbl, K., Clayman, R. V., McDougall, E. M., Urban, D. A., Gill, I. and Kavoussi, L. R.: Laparoscopic nephrouretectomy: evaluation of first clinical series. Eur. Urol., 23: 431, 1993. 7. Ono, Y., Katoh, N., Kinukawa, T., Sahashi, M. and Ohshima, S.: Laparoscopic nephrectomy, radical nephrectomy and adrenalectomy: Nagoya experience. J . Urol., 152 1962, 1994. 8. Eraky, I., El-Kappany, H., Shamaa, M. A. and Ghoneim, M. A.: Laparoscopic nephrectomy: an established routine procedure. J. Endourol., 8: 275, 1994. 9. Katoh, N., Ono, Y., Yamada, S., Kinukawa, T., Hattori, R. and Ohshima, S.: Laparoscopic radical nephrectomy for renal cell carcinoma: early experience. J . Endourol., 8: 357, 1994. 10. Gill, I. S., Kavoussi, L. R., Clayman, R. V., Ehrlich, R. M., Evans, R., Fuchs, G., Gershman, A,, Hulbert, J. C., McDougall, E. M., Rosenthal, T., Schuessler, W. W. and Shepard, T.: Complications of laparoscopic nephrectomy in the initial 185 patients: a
723
multi-institutional review. J. Urol., 154: 479, 1995. 11. Gaur, D. D., Agarwal, D. K. and Purohit, K. C.: Retroperitoneal laparoscopic nephrectomy: Initial case report. J . Urol., 149 103, 1993. 12. Rassweiler, J. J., Henkel, T. O., Stoch, C., Greschner, M., Becker, P., Preminger, G. M., Schulman, C. C., Frede, T. and Alken, P.: Retroperitoneal laparoscopic nephrectomy and other procedures in the upper retroperitoneum using a balloon dissection technique. Eur. Urol., 25: 229, 1994. 13. McDougall, E. M., Clayman, R. V. and Fadden, P. T.: Retroperitoneoscopy: the Washington University Medical School experience. Urology, 43: 446, 1994. 14. Ono, Y., Katoh, N., h n u k a w a , T., Matsuura, 0. and Ohshima, S.: Laparoscopic nephrectomy via a retroperitoneal approach. J. Urol., 156 1101, 1996. 15. McDougall, E. M., Clayman, R. V. and Eldshry, 0. M.: Laparoscopic radical nephrectomy for renal tumor: The Washington University experience. J. Urol., 155: 1180, 1996. 16. Urban, D. A., Kerbl, L., McDougall, E. M., Stone, A. M., Fadden, P. T. and Clayman, R. V.: Organ entrapment and renal morcellation: permeability studies. J . Urol., 1 5 0 1792, 1993. 17. Suzuki, K, Tanaka, T., Ikeda, R., Taniguchi, T., Ben, A.. Shiraiwa, K and Tsugawa, R.: Terumo guidewire in endourology treatment. J. Endourol., 3: 69, 1989. 18. Robson, C. J.: Radical nephrectomy for renal cell carcinoma. J. Urol., 8 9 37, 1963.
Prrrircrl
in
1I.S.A.
LAPAROSCOPIC RADICAL NEPHRECTOMY: THE NAGOYA EXPERIENCE YOSHINARI ONO, NORIO KATOH, TSUNEO KINUKAWA, OSAMU MATSUURA SHINICHI OHSHIMA
AND
Fro111 the Department of Urology, Komaki Shitrim Hospital, Okazaki City Hospital, and Shakar Hokeri C h u k w Hospital, Kornaki shi, Japan
ABSTRACT
Purpose: We evaluated the efficacy of laparoscopic radical nephrectomy for removing kidneys with small volume renal cell carcinoma. Materials and Methods: 25 patients (19 men and 6 women, mean age 59) who had a kidney with small volume renal cell carcinoma (diameter less than 5 cm.), underwent laparoscopic radical nephrectomy. The kidney was dissected laparoscopically together with the adrenal gland, perirenal fatty tissue and Gerota's fascia. In 11 patients, we used the transperitoneal approach and in the remaining 14 we used the retroperitoneal approach, in which a working space is created by finger and balloon dissection. We maneuvered the kidney into the laparoscopy sack, which was then removed through an additional 5 to 6 cm. incision. Results: All 25 kidneys were removed successfully. Mean operation time was 5.3 hours and mean estimated blood loss was 335 ml. There were 5 complications, including a patient who suffered an injury to the duodenum, which was treated by open duodenojejunostomy. Full convalescence occurred a t an average 23 days. No metastatic disease, no local recurrence and no seeding a t the port sites occurred during the followup of 7 to 49 months (mean, 22 months). Conclusions: Laparoscopic radical nephrectomy is recommended a s a minimally invasive procedure for removing kidneys with small volume renal cell carcinoma. KEYWORDS:carcinoma, renal cell, nephrectomy, laparoscopy
Laparoscopic nephrectomy has been performed to remove kidneys with various benign and malignant diseases since the first clinical success by Clayman e t al in July 1990.1-1" Although i t has been accepted as a minimally invasive procedure for removing kidneys with benign diseases, it is still controversial as a procedure for removing kidneys with malignant diseases. We started a laparoscopic nephrectomy program for benign renal diseases in July 1991.4 So far, 50 of 54 patients with severely damaged kidneys have been treated successfully.i.14 We started a laparoscopic radical nephrectomy program for malignant renal diseases in July 1992.' Under laparoscopic observation, we ligate the renal vessels and then dissect the kidney together with the adrenal gland, perirenal fatty tissue and Gerota's fascia. So far, 25 patients with small volume renal cell carcinomas have been treated. We present our procedure for laparoscopic radical nephrectomy and the clinical results for our 25 patients. MATERIALS A N D METHODS
Since July 1992, we have performed laparoscopic radical nephrectomy on 25 patients with small volume renal cell carcinomas of less than 5 cm. in diameter (see table). Initially, we used t h e previously described transperitoneal approach;2,7," our first 11 patients were treated in that way. Then, in September 1994, we developed the retroperitoneal approach; our next 14 patients were treated in this way. Between July 1992 and December 1995, we performed open radical nephrectomy on 17 patients with low stage renal cell carcinomas at our hospitals. We compared all data, including information on long-term recovery, that we obtained from our 2 groups of patients. Preoperative preparation. All 25 patients underwent bowel preparation as described previously.',7 I n t h e first 2 1 cases, the renal arteries were embolized the day before or the day of Accepted for publication January 10,1997.
surgery to minimize blood loss and to manage the great renal vessels more easily and quickly during surgery. This practice was abandoned in January 1996 because renal arterial embolization is invasive, and we had learned to manage the great renal vessels efficiently. After the induction of general anesthesia, patients who were undergoing a transperitoneal procedure were placed in a semilateral (70-degree)position, and patients undergoing a retroperitoneal procedure were placed in a lateral position. Radical nephrertomy via the transperitoneal approach. Operative procedures were described previously.'. After duodenum injury occurred because of the use of a 5 mm. Padron'* retractor, however, we have placed a 12 mm. trocar instead in the midclavicular line 5 to 6 cm. above the level of the umbilicus so t h a t we can now use a safer 10-mm. Padron retractor. Radical nephrectomy uia the retroperitoneal approach. A 3 cm. incision was made along t h e anterior axillary line 1 cm. below t h e level of the umbilicus. The external and internal oblique muscles and the transversus abdominalis were divided bluntly with retractors. The exposed Gerota's fascia was dissected digitally from the quadrant lumbotum and psoas muscle. A balloon, consisting of the middle finger of a size 8 surgeon's glove tied to t h e top of a rigid nephroscope, was placed behind the kidney and, under direct vision through the rigid nephroscope, was inflated with 1,000 ml. of normal saline to produce a working space. This inflation was maintained for 5 minutes to allow hemostasis to take place (fig. 1).After the peritoneum was digitally dissected medially from the abdominal wall, a 12 mm. trocar was inserted 5 to 6 cm. above the first incision (fig.2, B ) under digital control as described previously.'.' In the posterior axillary line, a 12 mm. trocar was placed at the level of the umbilicus (fig. 2, C ) and a 5 mm. trocar 5 to 6 cm. above the level of the umbilicus (fig. 2, D).In the midaxillary line, a 12 mm. trocar was placed
719
* damner Surgical Instruments Inc., Hawthorne,
New York.
720
LAPAROSCOPIC RADICAL NEPHRECTOMY Patients’ characteristics and results
.n. .
No.--AgeSex
Side
Owrative Time thrs.1
14 2 -52 3 -56 4 -51 5 -72 6 4 7 -50 8 -52 9 -52 10 4 1 11 4 3
-M -hi
Rt. Lt. Lt. Rt. Rt. Rt. Lt . Rt. Rt. Rt. Lt.
6.3 7.7 6.5 5.1 6.3 5.0 6.5 4.2 5.2 6.8 6.0
450 800 100 400 400 200 900 400 190 132 395
12 -74
-M
Rt. Rt. Rt . Rt. Rt. Lt. Lt. Rt. Rt. Rt . Rt . Rt . Lt. Lt.
3.7 3.9 5.2 5.5 5.3 4.0 3.0 6.4 4.8 6.9 4.3 4.1 5.0 5.9
100 50 100 290 279 700 145 480 96 386 160 50 618 552
-F -M
-M -M
-M -F -M
-M -M
13 4 8 -F
14 4 4 15 - 4 8 16 4 9 17 -70 18 -59 19 -56 20 -57 21 -48 22 -74 23 - 4 7 24 -77 25 4 8
-M -M
-M -F -F -M -M -M -F
-M -M -M
Estimated Blood Loss (rnl.1
Removal
Success Success Success Success Success Success Success Success Success Success Success
~
Complication
Tronspentoneal approach No Injury of spleen No No No No Injury of adrenal gland No Injury of duodenum No No Retroperitoneol approach Success No Success No Success No Success No Success No Success Bleeding from penureteric artery No Success Success No Success No Success No Success No Success No Success No
Success
Paralytic ileus
-
Pathological Findings i stage/gradel
Wt.
Renal cell Ca tpTlpNOG2l Renal cell Ca cpT2pNOGlI Renal cell Ca (pTlpNOC21 Renal cell Ca (pTlpNOG1) Renal cell Ca tpTLpNOG21 Renal cell Ca tpT2pNOC.2) Renal cell Ca tpT2pNOC.21 Renal cell Ca IpTLZpNOGlI Renal cell Ca (pT2pNOG21 Renal cell Ca ipT2pNOG21 Renal cell Ca tpT2pNOG2I
310 500 165 330 160 270 340 220 426 360 346
Renal cell Ca (pTlpNOG11 Renal cell Ca cpTZpN0G21 Renal cell Ca (pTlpNOG1 I Renal cell Ca (pTlpNOG21 Renal cell Ca (pT3pNOG2 I Renal cell Ca (pT2bpNOG21 Renal cell Ca (pT2pNOG2 I Renal cell Ca (pT2pNOG21 Renal cell Ca (pT2pNOG2) Renal cell Ca tpT2pNOG21 Renal cell Ca tpT2pNOGlI Renal cell Ca 1pT2pNOG21 Renal cell Ca (pT2pNOG21 Renal cell Ca loT3oNOG2 I
215 170 330 420 176 210 162 490 255 368 230 322 190 250
FIG. 1. Balloon dissection in retroperitoneal space. Balloon is inflated with 1,000 ml. of saline to produce working space in posterior aspect of kidney.
at the level of the umbilicus (fig. 2, E ) . A 12 mm. Origin* trocar was placed in the site of the first incision (fig. 2, A), which was sutured to prevent carbon dioxide leakage. Carbon dioxide insumation at a pressure of 12 mm. Hg maintained the working space in the retroperitoneal cavity. A 0-degree laparoscope was inserted through port A for observation, and a 10 mm. retractor was introduced through port B to deflect the peritoneum medially. The procedure for dissecting the kidney was basically the same as in the transperitoneal approach. The ureter was identified, exposed and dissected before being secured with ligature clips and transected with scissors. After retracting the kidney medially, the lateral wall of the vena cava or the aorta was dissected and exposed upward. Then the renal vessels were exposed and dissected. In cases of disease on the * Origin Medsystems Inc., Menlo Park, CA.
right side, the renal artery was secured with ligature clips before being transected with scissors and the adrenal arteries were divided by electrocautery. In cases of disease on the left side, the renal vein was secured and transected proximally to the left adrenal vein and the left gonadal vein by endoscopic gastrointestinal anastomosis vascular stapler, and the adrenal arteries were divided by electrocautery. In the anterior aspect of the kidney, the anterior lobe of Gerota’s fascia was dissected from the peritoneum. As we retracted the kidney downward, the right adrenal gland was dissected out from the liver, the diaphragm and the psoas muscle, and the left adrenal gland from the tail of the pancreas, the diaphragm and the psoas muscle. The double-layered laparoscopy sack of impermeable plastic and nondistensible nylon was equipped with a plasticcoated guide wire through its top that allowed us to open and
LAPAROSCOPIC RADICAL NEPHRECTOMY
721
ng the ureter. Hemostasis was achieved laparoscopically in :hese 3 cases, with 2 patients (cases 7 and 17) each requiring transfusion of 2 units of blood. Duodenal perforation was iiscovered in 1 patient on the day after surgery on the right side (case 9), when bile was discharged from the drainage tube. The injury might have been caused by a 5 mm. Padron endoscopic exposing retractor, although it had not been no/I I ticed during the laparoscopic surgery. The patient was treated successfully with open duodenojejunostomy. Three of the complications (cases 2, 7, 9) occurred during the transperitoneal procedure and 1 (case 17) during the retroperitoneal procedure. In 21 cases, the kidney could be entrapped in the laparosPosterior Anterior copy sack, but 4 kidneys (cases 9, 12, 16, 23) could not. In 1 Axillary Axillary patient, who was treated transperitoneally (case 9). the Line Line weight of the dissected mass was 426 gm. In the other 3 Line Line patients, who were treated retroperitoneally (cases 12, 16, FIG.2. Location of ports in transperitoneal (Zefl) and retroperito- 23), the weights of the dissected masses were 215, 176 and neal (right) radical nephrectomy. 322 gm., respectively. However, in these cases, the working space was too small to entrap the kidneys. The 4 kidneys close it firmly.14.16.17Trocar A was removed and the sack was were removed by hand through the enlarged first incision, introduced into the working space through this first incision, which in 2 cases was further enlarged by about 2 cm. and which was then closed again. After renewed carbon dioxide kept open with retractors. Operative time was between 3 and 7.7 hours (mean 5.3 insufflation, the specimen that included the kidney, the adrenal gland, perirenal fatty tissue and Gerota's fascia was hours); in the transperitoneal approach it was between 4.2 maneuvered together into the sack under laparoscopic obser- and 7.7 hours (mean, 6 hours) and in the retroperitoneal vation without being morseled or minced. The sack was approach it was between 3 and 6.9 hours (mean, 4.9 hours). pulled out through the first incision, which was enlarged Overall estimated blood loss was between 50 and 900 ml. vertically toward port B by an additional 5 to 6 cm. skin and (mean 335 ml.); in the transperitoneal approach, it was bemuscle incision in the transperitoneal approach, and an ad- tween 100 and 900 ml. (mean 397 ml.), and in the retroperditional 5 to 6 cm. skin incision and blunt abdominal muscle itoneal approach, it was between 50 and 700 ml. (mean 285 division in the retroperitoneal approach. The incision was m1.h Postoperatively, an average of 43 mg. of pentazocine closed by 2 layers of interrupted muscle suture and inter- w a s given intramuscularly to 20 patients and the remaining rupted skin suture. As the 4 other trocars were removed, a 5 patients did not request analgesics. There was only 1 comPenrose* drain was routinely placed through port E in the plication in the early postoperative period. One patient (case renal bed to determine postoperative blood loss. The drainage 25) had paralytic ileus, which was successfully treated by tube was removed 1 or 2 days later as described previ~usly.~ conservative therapy. Postoperative hospital stay was between 7 and 17 days (mean l l days), and full convalescence occurred between days 16 and 46 (mean day 23). These figRESULTS ures exclude the patient (case 9) who underwent duodenojeThe 11 patients (9 men and 2 women) who underwent jenostomy, stayed in the hospital for 30 days after the surtransperitoneal laparoscopic radical nephrectomy were be- gery, and achieved full convalescence on day 45. There were tween 44 and 83 years old (mean age 57). Seven patients had no differences in the administration of analgesics, hospital disease on the right side and 4 had disease on the left side. stay and the period to full convalescence between the paThe preoperative diagnosis was TlNOMO disease in 3 pa- tients treated transperitoneally and those treated retroperitients and T2NOMO disease in 8 patients. No patient had toneally. undergone abdominal surgery. All 25 specimens were removed intact without being morThe 14 patients (10 men and 4 women) who underwent seled or minced. Their weight was between 162 and 500 gm. retroperitoneal laparoscopic radical nephrectomy were be- (mean 289 gm.), and the tumor size was between 20 X 20 x tween 48 and 77 years old (mean age 60). Ten patients had 20 mm. and 50 x 40 x 40 mm. The number of removed lymph disease on the right side and 4 patients had disease on the nodes was between 1 and 10 (mean 4). none of which had left side. The preoperative diagnosis was TlNOMO disease in metastasis. Final pathological analysis revealed that the re2 patients and T2NOMO disease in 12 patients. Four patients nal cell carcinoma was stage pT1 in 6, pT2 in 17, and pT3a in had undergone abdominal surgery; one patient (case 16) with 2 patients. The followup period was between 7 and 49 months an affected right native kidney had received a renal trans- (mean 22), and no patient had a metastatic disease, a local plant, and the other 3 patients had had open transperitoneal recurrence or seeding at the port sites. hysterectomy (case 18), open colectomy (case 20) and open The 17 patients (12 men and 5 women) who underwent radical prostatectomy (case 24). Statistical analysis was per- open radical nephrectomy were between 44 and 80 years old formed with Student's t test. (mean age 61).Ten patients had disease on the right side and All 25 kidneys were dissected successfully and completely 7 had disease on the left side. Two patients had pTlpNOpMO through either the transperitoneal or the retroperitoneal ap- disease and 15 had pT2pNOpMO disease. The weights of the proach. Of the 14 retroperitoneal cases that included 4 pa- specimens were between 300 and 504 gm. (mean 375 gm.). tients with previous abdominal surgery, balloon dissection Operative time was between 3 and 5.6 hours (mean 3.6), successfully created a working space without causing any which was shorter than in the laparoscopically treated group bleeding. It took 0.4 to 0.7 hours (mean 0.6 hours) to create (p <0.001). Blood loss was between 141 and 844 ml. (mean the retroperitoneal working space. 474). There was no significant difference between the 2 There were 4 intraoperative complications: bleeding from groups. Postoperatively, a n average of 63 mg. pentazocine an injured spleen (case 2) and an injured adrenal gland (case was given intramuscularly to all 17 patients, which was a 7),both caused by improper retraction, and bleeding from a n larger dose than in the group treated laparoscopically (p injured periureteral artery (case 17) caused by the clip secur- <0.01). There were 2 complications. Two patients had paralytic ileus, which could successfully be treated by conserva* Fuji Systems Co., Tokyo, Japan.
I
I
I
\
I
722
LAPAROSCOPIC RADICAL NEPHRECTOMY
tive therapy. Postoperative hospital stay was between 15 and 35 days (mean 24), which was significantly longer than in the group treated laparoscopically ( p <0.001). Full convalescence occurred between days 42 and 90 (mean day 64), which was also significantly longer than in the group treated laparoscopically ip < 0 . 0 0 1 ~ I~lscrssIo~ Radical nephrectomy has been the standard treatment for localized renal cell carcinoma since the initial report by Robson in 1963.'* The procedure includes ligation of the renal vessels before manipulation of the tumor, removal of the kidney and adrenal gland together with the perirenal fatty tissue and Gerota's fascia, and lymph node dissection. We first performed radical nephrectomy as a laparoscopic procedure in July 1992,2 when we removed a kidney with a small volume renal cell carcinoma. A total of 25 patients with a renal cell carcinoma of less t h a n 5 cm. in diameter has been treated in this manner. In our laparoscopic procedures, ligation of the renal vessels is accomplished by early identification of the ureter and cephalad dissection along the great vessels without manipulation of the tumor. The removal of the kidney and adrenal gland together with the penrenal fatty tissue and Gerota's fascia is also accomplished without technical difficulty. However, laparoscopic lymph node dissection cannot be performed at present and it is particularly difficult in cases with disease on the right side. This is why we choose laparoscopic radical nephrectomy only for cases of small volume renal cell carcinoma, which do not normally have microscopic lymph node involvement. I n our series, mean operative time was 5.3 hours, mean estimated blood loss was 335 ml., and there were 4 intraoperative and 1 postoperative complications. These results are not as good as those of the open procedure. Three of the 4 intraoperative complications occurred in the first group of patients who were treated transperitoneally. They were caused by improper retraction of intra-abdominal organs. After the duodenum injury occurred, we used a 10 mm. instead of a 5 mm. Padron retractor, which reduces the risk of injury to intra-abdominal organs such as the duodenum and spleen. Learning curve effects have helped us improve our operative techniques. McDougall et al described several postoperative complications, such as heart failure and wound hernia, which, fortunately, we did not see in our patients.I3 Although 1 patient was hospitalized longer with a complication, the other 24 patients treated by laparoscopic surgery recovered faster and returned to their normal activities earlier than the 17 patients treated by open surgery. No metastatic disease, no local recurrence and no port site seeding was found in 7 to 49 months of followup (mean 22). These data suggest that laparoscopic radical nephrectomy is a minimally invasive procedure to be recommended for removing kidneys with small volume renal cell carcinoma. As with laparoscopic simple nephrectomy, laparoscopic radical nephrectomy was first performed via the transperitoneal approach. In our series, the first 11 patients were treated transperitoneally. The problems we encountered, such as injury to intra-abdominal organs and the difficulty of retracting them, are inherent to the transperitoneal approach. We therefore applied the retroperitoneal approach to laparoscopic radical nephrectomy. Between September 1994 and January 1996, the next 14 patients were treated retroperitoneally. We encountered only 1 problem, an injury to the periureteral artery. We also successfully removed kidneys from patients with a history of abdominal surgery. We modified Gaur's original retroperitoneal method. 1.1 We made the first 3 cm. incision in the anterior axillary line 1 cm. below the level of the umbilicus, which greatly facilitates the establishment of the ports in the anterior axillary line. We used a balloon tied to the top of a rigid nephroscope for
dissection when creating the retroperitoneal working space, because the position of the balloon can be controlled easily and because the progress of dissection can be monitored under direct vision. We performed finger and balloon dissection only in the posterior aspect of the kidney, however, because this technique does not allow the exact dissection of the Gerota's fascia from t h e peritoneum and poses the threat of injury to both; we used laparoscopic forceps instead. As have other groups,1o we encountered injuries to abdominal organs in our transperitoneal approach. I n contrast, we encountered no injuries to abdominal organs in our retroperitoneal approach. There is obviously less risk of injury to abdominal organs when all manipulations are restricted to the retroperitoneal space. Our retroperitoneal procedures had a shorter mean operating time than the transperitoneal procedures we or other groups performed.11-'4 Creating a working space in the retroperitoneal cavity was time-consuming but subsequently allowed easy dissection of the ureter and renal vessels. The retroperitoneal approach also makes some transperitoneal maneuvers redundant, such as the incision of the peritoneum and the dissection of the posterior aspect of the kidney. Lesser risk of injury to abdominal organs and shorter OPerative time seem to be advantages of the retroperitoneal approach. However, our series was not a randomized study and the retroperitoneally treated patients have benefited from our learning curve. Thus we must not draw final conclusions about the efficacy of the retroperitoneal approach in laparoscopic radical nephrectomy. The working space created retroperitoneally is smaller than the one available transperitoneally, which makes the entrapment of the renal specimen more difficult even in simple n e p h r e ~ t o m y .14~ ~I.n our 14 retroperitoneal radical nephrectomies, we encountered 3 cases in which the successfully dissected mass could not be reduced in size and could not be entrapped in the sack because the working space was too small. We had to enlarge the original incision, which erased the greatest advantage of laparoscopic radical nephrectomy, that is its minimally invasive nature. The small working space could be the critical disadvantage of the retroperitoneal approach in laparoscopic radical nephrectomy. Large kidneys should therefore be removed by transperitoneal laparoscopic radical nephrectomy or by the combined method of McDougall et al, who open t h e peritoneum to obtain a sufficiently large working space after dissection of the kidney through the retroperitoneal approach. 1:' Our current work focuses on t h e advantages and disadvantages of morseling and mincing the dissected mass as means of preserving minimal invasiveness. CONCLUSIONS
Our results support previous reports", t h a t recommend laparoscopic radical nephrectomy for removing kidneys with small volume renal cell carcinomas. However, it is necessary to gather more long-term data on patients to determine whether laparoscopy is superior to open surgery in radical nephrectomy. The retroperitoneal approach should be selected when the patient has a history of abdominal surgery or when the condition indicates that a shorter operating time is important. REFERENCES
1. Clayman, R. V., Kavoussi, L. R., Soper, N. J., Dierks, S. M., Meretyk, S., Darcy, M. D., Roemer, F. D., Pingleton, E. D., Thomson, P. G . and Long, S. R.: Laparoscopic nephrectomy: Initial case report. J. Urol., 146: 278, 1991. 2. Ono, Y., Sahashi, M., Yamada, S. and Ohshima. S.: Laparoscopic nephrectomy without morcellation for renal cell carcinoma: Report of initial 2 cases. J. Urol., 1 5 0 1222, 1993. 3. Terachi. T.. Matsuda, T., Kawakita. M., Mikami. O., Hoiii, Y.,
LAPAROSCOPIC RADICAL NEPHRECTOMY Ogura, K., Takeuchi, H., Komatsu, Y. and Yoshida, 0.:Laparoscopic nephrectomy: A report of 13 cases. Jap. J. Endourol. ESWL, 6: 133, 1993. 4. Katoh, N., Ono, Y., Yamada, S., Kinukawa, T., Sahashi, M., Matsuura, M., Hirabayashi, S., Hatano, Y., Sakakibara, T. and Ohshima, S.: Review of laparoscopic nephrectomy in 26 patients. J a p . J. Endourol. ESWL, 6 129, 1993. 5. Kavoussi, L. R., Kerbl, K., Capelouto, C. C., McDougall, E. M. and Clayman, R. V.: Laparoscopic nephrectomy for renal neoplasms. Urology, 42: 603, 1993. 6 . Kerbl, K., Clayman, R. V., McDougall, E. M., Urban, D. A., Gill, I. and Kavoussi, L. R.: Laparoscopic nephrouretectomy: evaluation of first clinical series. Eur. Urol., 23: 431, 1993. 7. Ono, Y., Katoh, N., Kinukawa, T., Sahashi, M. and Ohshima, S.: Laparoscopic nephrectomy, radical nephrectomy and adrenalectomy: Nagoya experience. J . Urol., 152 1962, 1994. 8. Eraky, I., El-Kappany, H., Shamaa, M. A. and Ghoneim, M. A.: Laparoscopic nephrectomy: an established routine procedure. J. Endourol., 8: 275, 1994. 9. Katoh, N., Ono, Y., Yamada, S., Kinukawa, T., Hattori, R. and Ohshima, S.: Laparoscopic radical nephrectomy for renal cell carcinoma: early experience. J . Endourol., 8: 357, 1994. 10. Gill, I. S., Kavoussi, L. R., Clayman, R. V., Ehrlich, R. M., Evans, R., Fuchs, G., Gershman, A,, Hulbert, J. C., McDougall, E. M., Rosenthal, T., Schuessler, W. W. and Shepard, T.: Complications of laparoscopic nephrectomy in the initial 185 patients: a
723
multi-institutional review. J. Urol., 154: 479, 1995. 11. Gaur, D. D., Agarwal, D. K. and Purohit, K. C.: Retroperitoneal laparoscopic nephrectomy: Initial case report. J . Urol., 149 103, 1993. 12. Rassweiler, J. J., Henkel, T. O., Stoch, C., Greschner, M., Becker, P., Preminger, G. M., Schulman, C. C., Frede, T. and Alken, P.: Retroperitoneal laparoscopic nephrectomy and other procedures in the upper retroperitoneum using a balloon dissection technique. Eur. Urol., 25: 229, 1994. 13. McDougall, E. M., Clayman, R. V. and Fadden, P. T.: Retroperitoneoscopy: the Washington University Medical School experience. Urology, 43: 446, 1994. 14. Ono, Y., Katoh, N., h n u k a w a , T., Matsuura, 0. and Ohshima, S.: Laparoscopic nephrectomy via a retroperitoneal approach. J. Urol., 156 1101, 1996. 15. McDougall, E. M., Clayman, R. V. and Eldshry, 0. M.: Laparoscopic radical nephrectomy for renal tumor: The Washington University experience. J. Urol., 155: 1180, 1996. 16. Urban, D. A., Kerbl, L., McDougall, E. M., Stone, A. M., Fadden, P. T. and Clayman, R. V.: Organ entrapment and renal morcellation: permeability studies. J . Urol., 1 5 0 1792, 1993. 17. Suzuki, K, Tanaka, T., Ikeda, R., Taniguchi, T., Ben, A.. Shiraiwa, K and Tsugawa, R.: Terumo guidewire in endourology treatment. J. Endourol., 3: 69, 1989. 18. Robson, C. J.: Radical nephrectomy for renal cell carcinoma. J. Urol., 8 9 37, 1963.