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Laparoscopic Partial Nephrectomy in Cold Ischemia:: Renal Artery Perfusion
0022-5347/04/1711-0068/0 THE JOURNAL OF UROLOGY® Copyright © 2004 by AMERICAN UROLOGICAL ASSOCIATION
Vol. 171, 68 –71, January 2004 Printed in U.S.A.
DOI: 10.1097/01.ju.0000101040.13244.c4
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA: RENAL ARTERY PERFUSION ¨ NTER JANETSCHEK,* ALAA ABDELMAKSOUD, FARIBORZ BAGHERI, HASSAN AL-ZAHRANI, GU KARL LEEB AND MANFRED GSCHWENDTNER From the Departments of Urology and Radiology (MG), Elisabethinen Hospital, Linz, Austria
ABSTRACT
Purpose: Laparoscopic partial nephrectomy represents a feasible option for patients with small renal masses. We describe our initial experience with laparoscopic partial nephrectomy in cold ischemia achieved by renal artery perfusion. Materials and Methods: From November 2001 to March 2003 laparoscopic partial nephrectomy in cold ischemia was performed in 15 patients with renal cell carcinoma. Cold ischemia was achieved by continuous perfusion of Ringers lactate at 4C through the renal artery, which was clamped. Tumor excision was performed in a bloodless field with biopsy taken from the tumor bed. The collecting system was repaired if needed. Renal reconstruction was performed by suturing over hemostatic bolsters. Results: All procedures were successfully completed laparoscopically by our new technique. Mean operative time was 185 minutes (range 135 to 220). Mean ischemia time was 40 minutes (range 27 to 101). Estimated mean intraoperative blood loss was 160 ml (range 30 to 650). Entry to the collecting system in 6 patients was repaired intraoperatively. Additional vascular repair was done in 2 patients. There were no significant postoperative complications. Postoperative followup in 8 patients showed that the renal parenchyma was not damaged by the ischemic period. Conclusions: Our initial experience of incorporating cold ischemia via arterial perfusion into laparoscopic partial nephrectomy shows the feasibility and safety of the technique. We believe that this approach has the potential to make laparoscopic partial nephrectomy for renal cell carcinoma safe and reliable. KEY WORDS: kidney; nephrectomy; laparoscopy; carcinoma, renal cell; renal artery
offers the surgeon extra time and, therefore, it has become the standard procedure during open surgery. To achieve results comparable to those of open surgery cold ischemia had to be integrated into laparoscopy. The feasibility of laparoscopic renal surface hypothermia by applying ice slush and renal hypothermia by retrograde ureteral cold saline perfusion, respectively, was already reported by others.11, 12 We present our first experience with renal cooling during laparoscopic surgery for small RCCs by cold arterial perfusion.
Within a short period laparoscopic radical nephrectomy for renal cell carcinoma (RCC) has become a standard of care.1 However, because of the widespread use of imaging techniques such as ultrasonography and computerized tomography (CT), a large number of small, localized renal tumors is detected incidentally.2 For such patients organ sparing surgery must be considered as an alternative to radical nephrectomy even if the contralateral kidney functions normally.3 Due to encouraging reports about tumor recurrence and cancer specific survival in cases of nephron sparing surgery (NSS), it is not unlikely that partial nephrectomy may become more frequent than radical nephrectomy in the future.3, 4 In 1993 the first laparoscopic partial nephrectomy in a porcine model was reported.5 At many centers groups have since developed their techniques to perform NSS by laparoscopy.6 – 8 We have previously described a technique to perform wedge resection for RCC by laparoscopy.9 However, this technique was restricted to tumors 2 cm or less since it was performed without inducing renal ischemia. To duplicate all principles of open surgery by laparoscopy we changed our technique by introducing renal ischemia and suture repair of the collecting system and renal parenchyma, as described by Gill et al.10 So-called warm ischemia is achieved by temporary occlusion of the renal artery alone or the artery and vein together. The time available to do partial resection and repair the collecting system and parenchyma during warm ischemia is limited and the surgeon must race against the clock. Renal cooling during ischemia protects the kidney,
MATERIALS AND METHODS
From November 2001 to March 2003 laparoscopic partial nephrectomy under cold ischemia was performed in 15 patients. During this period only 3 partial resections were performed without cooling the kidney and no open NSS was done. Table 1 lists patient demographics. The indication was suspected RCC with a mean tumor size of 2.7 cm (range 1.5 to 4). The indication was elective in 14 patients. In 1 patient with bilateral RCC the smaller tumor was removed by wedge resection and laparoscopic contralateral nephrectomy was performed 8 weeks later. Table 2 shows tumor locations. Four tumors were completely intrarenal, including 2 confined within the lower pole and 2 that were central. Metastatic evaluation was negative and all tumors were clinically T1, N0, M0. In all patients preoperative angiomagnetic resonance imaging was performed to assess the number and location of the renal arteries. Preoperative renal scintigraphy (mercaptoacetyltriglycine clearance for split renal function) was done to obtain baseline data on renal function for followup. Informed consent was obtained for the possibility of conversion to laparoscopic radical or open partial nephrectomy.
Accepted for publication August 22, 2003. * Correspondence: Department of Urology, Elisabethinen Hospital, A-4010 Linz, Postfach 239, Fadinger Strasse 1Austria (telephone: ⫹43-732-7676-4555; FAX: ⫹43-732-7676-4556; e-mail: [email protected]). 68
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA TABLE 1. Patient demographic Features Total No. pts No. men/women Mean age (range) Mean kg body wt (range) Mean mg/dl preop. serum creatinine (range) No. lesion side (%): Lt Rt
15 9/6 58 (36–76) 85.4 (57–130) 1.1 (0.91–1.30) 11 (73) 4 (27)
TABLE 2. Tumor location
Anterior Posterior Lat Medial
No. Upper Pole (side)
No. Middle Third (side)
No. Lower Pole (side)
1 (lt)
1 (rt) 1 (lt) 1 (lt) 3 (lt)
1 (lt) 4 (lt) 1 (rt)
2 (rt)
Technique. Preoperative preparation and anesthesia induction were done as usual. Placement of an open tip ureteral catheter, usually a single pigtail catheter, was done under fluoroscopy to be used later to determine collecting system integrity. An angiocatheter was then passed into the main renal artery through a femoral puncture on the ipsilateral side. To avoid dislodging the catheter this procedure was done by an interventional radiologist in the theater with the patient on the operating table. The patient was then brought to the 45-degree lateral decubitus position. In this final position for laparoscopic surgery the angiocatheter was again assessed and advanced in the renal artery close to the origin of the segmental arteries if needed. The approach to the kidney was transperitoneal in 14 patients and retroperitoneal in 1. Port placement varied according to tumor location. In addition to the 4 trocars usually required for radical nephrectomy, that is for the camera a 10 mm, for the right and left surgeon hands a 5 and a 10 mm, and for the retractor a 10 mm trocar, an additional 10 mm trocar for the tourniquet was placed in the lower abdomen. The thermoprobe was introduced through the sheeth of a Veress needle. The number of trocars was the same for the transperitoneal approach and retroperitoneoscopy. In the first 2 patients the renal hilum was not dissected and the renal artery was occluded by a balloon integrated into the angiocatheter. However, since some arterial bleeding occurred in the second patient, we preferred to use a tourniquet for artery occlusion in the following 13, which proved to be much safer. Therefore, an angiocatheter without a balloon was used. The renal artery was secured and later occluded using a tourniquet of 5 mm umbilical tape and a 10Fr silicone tube, which was placed as close to the origin of the artery as possible. We were prepared to occlude additional smaller arteries with laparoscopic bulldog clamps but it has not been required to date. Initially the renal vein was secured medial to the gonadal, lumbar and adrenal veins but not occluded in 11 patients, also using umbilical tape. However, we stopped securing the renal vein since there was no venous backflow due to the positive pressure of perfusate in the vein. Intravenous infusion of 200 cc 20% mannitol was given 15 minutes before arterial occlusion. After approaching the tumor the overlying fat was dissected and the renal capsule around the tumor was incised using a monopolar hook. Cold ischemia was then started. It was achieved by occluding the renal artery and perfusing 1,000 ml iced Ringers lactate at 4C at a rate of 50 ml per minute through the angiocatheter. Surgery was started immediately following the initiation of cold perfusion. Because of availability, 3 Infusomat fm (Braun, Meldungen, Germany) perfusion pumps were used simultaneously to achieve the required perfusion rate. Mannitol (100 ml 20%) was added to each 1,000 ml Ringers
69
lactate to achieve an osmolality of 430 mOsm/ml to avoid parenchymal edema.11 Renal temperature was continuously monitored with a thermocouple probe residing in the parenchyma. When a parenchymal temperature of 25C was attained, perfusion was decreased to maintain a steady state. The patient was warmed with a Bair Hugger (Augustine Medical Inc. Eden Prairie) warm air blanket and the temperature was continuously monitored by a thermocouple probe residing in the nasopharynx. Tumor excision was performed in a blood-free field using scissors but no diathermy (fig. 1). Biopsy was taken from the tumor bed. The tumor and overlying fat were placed in separate organ bags, which were removed later. The integrity of the collecting system was evaluated by injecting methylene blue through the pre-placed ureteral catheter. Occasionally injured large vessels in the tumor bed were clearly observed by a jet of perfusate. Therefore, the collecting system and injured vessels could be precisely repaired by figure-of-8 sutures using 4-zero polyglactin on a 17 mm 1/2 C needle (figs. 2 and 3). The cut edges of the parenchyma were approximated by 2 or 3 figure-of-8 sutures over a TapoTamb (Ethicon Sarl, Neuchatel, Switzerland) hemostatic bolster using zero polyglactin on a 36.4 mm needle (fig. 4). Fibrin glue (Baxter AG, Vienna, Austria) or a strip of a Tachocomb (Nycomed, Linz, Austria) was applied on the cut surface to avoid delayed bleeding. A tube drain was always left in place. Renal artery perfusion was terminated after the parenchymal sutures were tied. The renal artery catheter was removed following laparoscopic surgery. The arteriotomy was closed by a Perclose A-T (Abbott Vascular, Redwood City, California) percutaneous suture device. The urethral and ureteral catheters were removed on postoperative day 2 but they could be removed earlier if preferred. CT and renal scans were repeated 3 months postoperatively to document complete tumor removal, the integrity of repair and kidney function. RESULTS
Preoperative assessment of the arteries by angio-magnetic resonance imaging was always correct. Wedge resection was performed in 11 patients, major transverse resection was done in 2 and partial nephrectomy for central tumors was done in another 2 (figs. 1 and 3). These procedures were successfully terminated without conversion. Tourniquet placement was always possible without any problem. Tumor location was more important in regard to technical difficulty than the involved side. However, dissection of the right renal artery had to be performed in the interaortocaval space because of early artery
FIG. 1. Major transverse resection of lower right kidney pole
70
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA
FIG. 2. Left kidney. A, entry to collecting system is evidenced by methylene blue leakage. B, suture repair of collecting system with jet of perfusate issuing from cut vessel on tumor bed.
FIG. 3. Suture repair of left kidney (K) renal vein (V) in complete bloodless field after resection of centrally located tumor. R, renal parenchyma resection margin.
minutes. In 2 patients the thermocouple probe was dislodged during surgery. Mean laparoscopic operative time was 185 minutes (range 135 to 220). Ten to 20 minutes (mean 16) must be added for angiocatheter placement. Mean total ischemia time was 40 minutes (range 27 min to 101). The mean amount of perfusate was 1,580 ml (range 1,150 to 2,800). The mean decrease in body temperature during cold perfusion was 0.64C (range 0.5 to 1.1). Mean intraoperative blood loss was 160 ml (range 30 to 650). In 2 patients we noted high blood loss, which was due to insufficient balloon occlusion in 1 and intermittent perfusion pump failure in 1, which resulted in venous backflow from the injured renal vein. Only 1 patient required intraoperative blood transfusion. In another patient continuous flow of blood through the drain was observed postoperatively. Hemoglobin and hematocrit decreased to 9.9 gm/dl and 29.3%, respectively. Therefore, second look laparoscopy was performed on postoperative day 1. A suture had torn through the parenchyma. Surprisingly only little bleeding was observed at the operative site. The defect was covered by stripes of Tachocomb (Nycomed, Linz, Austria). Entry to the collecting system in 6 patients was repaired intraoperatively (fig. 2). Repair of the renal vein, segmental vein and artery was done in 2 patients in whom the tumors were located centrally, close to the hilum (fig. 3). Drainage was removed when its output was less than 50 ml per 24 hours. Mean hospital stay was 9.4 days (range 7 to 14). No urinary fistula or urinoma was observed. No postoperative morbidity due to puncture of the femoral artery or to the amount of perfusate was observed. Histopathological examination revealed RCC in 13 patients and angiomyolipoma in 2. Resection margins were negative in 14 patients. In 1 case a negative margin was not described where the tumor was in direct contact with the renal vein. During resection the vein was entered and repaired (fig. 3). To date postoperative renal function was evaluated in 8 patients. In 5 patients the decrease in renal function was 1%, 1%, 2%, 3% and 8%, respectively, on renal scintigraphy. In 3 patients followed elsewhere CT showed undisturbed perfusion of the renal parenchyma.
FIG. 4. Left kidney after complete parenchymal repair with sutures over hemostatic bolster.
DISCUSSION
branching. Angiocatheter dislodgment during dissection never occurred. Surgery was started immediately following the initiation of cold perfusion. It required about 10 minutes for the parenchymal temperature to decrease to 25C. To maintain the steady state of 25C the perfusion rate was decreased from 50 to 25 to 33 ml per minute. In 1 patient perfusion was inadequate because the catheter tip was not advanced beyond the tourniquet. However, in this patient total ischemia time was only 32
Laparoscopic NSS without renal ischemia is feasible and it can be achieved by step-by-step resection and hemostasis.9, 13 However, this technique has its drawbacks. It is restricted to tumors 2 cm or less in a favorable peripheral location and hemostasis is slow and tedious. Since the cut surface is continuously covered with blood and burned by extensive monopolar and bipolar coagulation, the distinction between tumor and normal renal tissue becomes difficult. It may compromise complete tumor resection. Necrotic urinary fistula due to diathermy close to the collecting system has been
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA
described.13 These reasons were why we replaced this technique with partial nephrectomy under cold ischemia. During ischemia the tissue is cut sharply in a blood-free field, avoiding diathermy. Normal renal tissue and tumor can be distinguished precisely, so that complete tumor resection can be continuously monitored. As in open surgery, hemostasis relies on suturing the cut edges of the parenchyma on bolsters of hemostatic material.10 A major restriction of this technique is time because renal damage is expected if ischemia time is longer than 30 minutes. Therefore, cooling the kidney, as in open surgery, is required if ischemia time is anticipated to be more than 30 minutes, as for larger tumors and tumors at unfavorable sites. In addition, unexpected problems during surgery may extend the operative time. The optimum temperature for hypothermic preservation is 15C, based on the canine experiments of Ward.14 A temperature of 20 to 25C is easier to maintain. Animal15 and human16, 17 studies have shown that this level of hypothermia provides complete renal protection from ischemia for at least 90 minutes. In situ renal hypothermia can be achieved with external surface cooling or perfusion of the kidney. These 2 methods are equally effective.15, 18, 19 The feasibility of surface cooling with ice slush by laparoscopy was reported recently.11 We chose the other alternative, namely arterial perfusion, because with this technique the laparoscopic part of the operation does not differ much from partial nephrectomy in warm ischemia. All necessary maneuvers are performed prior to surgery, so that the laparoscopic procedure is not rendered more complicated. Another innovative alternative was recently described. In 1 patient renal hypothermia was achieved by cold saline perfusion via the collecting system and a renal cortical temperature of 24C was achieved.12 Cold arterial perfusion has several advantages. A renal parenchymal temperature of 25C can be achieved rapidly. Therefore, tumor resection and parenchymal repair can be done at leisure in a clear, blood-free field. Due to positive perfusate pressure within the collecting system no venous backflow occurs. Continuous leakage and sometime even jets of perfusate do not disturb exposure, but rather allow us to identify cut and injured arterial and venous vessels in a completely blood-free field. In 2 complicated, centrally located tumors vascular lesions had to be repaired after removing the tumor, which was greatly facilitated by this effect. The use of a tourniquet to occlude the renal artery is probably mandatory to avoid an intimal lesion. However, we believe that a tourniquet is safer than a vascular clamp since it does not slide off and the artery can be re-occluded at any time in case of an emergency due to inadvertent bleeding. Damage to the renal parenchyma due to ischemia was not observed in any patient. However, there are several potential drawbacks to the method. Additional administration of intravenous fluids during surgery must be minimized to avoid fluid overload. Therefore, diuresis was induced directly after ischemia and no cardiopulmonary problems occurred. One should be aware of this specific risk in a solitary kidney, where fluid overload could theoretically be avoided by perfusate drainage through the cut left gonadal vein or venotomy. Dislodging the arterial catheter has been described.16 We never experienced this problem since the angiocatheter was introduced in the theater at the operating table and the catheter tip was advanced as far as possible. In this series we did not note a kidney with 2 or more arteries, compromising cooling. However, we were prepared to cannulate 2 arteries of equal size or perfuse the largest artery, while occluding the others with bulldog clamps. The cost factor may be a problem, according to the health system. Costs are increased since a radiologist is required in the theater and operative time is increased by about 20 minutes. In experienced hands the majority of laparoscopic partial nephrectomies can be performed in warm ischemia within 30 minutes. However, if an unexpected problem arises, irreversible
71
function of the kidney is at risk. Cold ischemia by whatever method decreases this risk and allows the less skilled laparoscopist to perform this type of surgery. In addition, the scope of indications is increased for the experienced laparoscopist. CONCLUSIONS
Our initial experience with incorporating cold ischemia via arterial perfusion into laparoscopic partial nephrectomy shows the feasibility and efficacy of this technique. This approach allows the duplication of the principles of the open surgery and makes laparoscopic NSS for RCC safe and reliable. It also facilitates vascular repair during surgery for difficult central tumors. REFERENCES
1. Chan, D. Y., Cadeddu, J. A., Jarrett, T. W., Marshall, F. F. and Kavoussi, L. R.: Laparoscopic radical nephrectomy: cancer control for renal cell carcinoma. J Urol, 166: 2095, 2001 2. Lightfood, N., Conlon, M., Kreiger, N., Bissett, R., Desai, M., Warde, P. et al: Impact of noninvasive imaging on increased incidental detection of renal cell carcinoma. Eur Urol, 37: 521, 2000 3. Herr, H. W.: Partial nephrectomy for unilateral renal cell carcinoma and a normal contralateral kidney: 10-year followup. J Urol, 161: 33, 1999 4. Fergany, A. F., Hafez, K. S. and Novick, A. C.: Long-term results of nephron sparing surgery for localized renal cell carcinoma: 10-year followup. J Urol, 163: 442, 2000 5. McDougall, E. M., Clayman, R. V., Chandhoke, P. S., Kerbl, K., Stone, A. M., Wick, M. R. et al: Laparoscopic partial nephrectomy in the pig model. J Urol, 149: 1633, 1993 6. Winfield, H. N., Donovan, J. F., Lund, G. O., Kreder, K. J., Stanley, K. E., Brown, B. P. et al: Laparoscopic partial nephrectomy: initial experience and comparison to the open surgical approach. J Urol, 153: 1409, 1995 7. Rassweiler, J. J., Abbou, C., Janetschek, G. and Jeschke, K.: Laparoscopic partial nephrectomy. The European experience. Urol Clin North Am, 27: 721, 2000 8. McDougal, E. M., Elbahnasy, A. M. and Clayman, R. V.: Laparoscopic wedge resection and partial nephrectomy—the Washington University experience and review of the literature. JSLS, 2: 15, 1998 9. Janetschek, G., Daffner, P., Peschel, R. and Bartsch, G.: Laparoscopic nephron sparing surgery for small renal cell carcinoma. J Urol, 159: 1152, 1998 10. Gill, I. S., Desai, M. M., Kaouk, J. H., Meraney, A. M., Murphy, D. P., Sung, G. T. et al: Laparoscopic partial nephrectomy for renal tumor: duplicating open surgical techniques. J Urol, 167: 469, 2002 11. Abreu, S. C., Gill, I. S., Ng, C., Mihir, D., Steinberg, A., Ramani, A. et al: Technique of laparoscopic renal hypothermia for partial nephrectomy. J Urol, suppl., 169: 20, abstract V77, 2003 12. Landman, J., Venkatesh, R., Lee, D., Vanlangendonck, R., Morissey, K., Andriole, G. L. et al: Renal hypothermia achieved by retrograde endoscopic cold saline perfusion: technique and initial clinical application. Urology, 61: 1023, 2003 13. Jeschke, K., Peschel, R., Wakonig, J., Schellander, L., Bartsch, G. and Henning, K.: Laparoscopic nephron-sparing surgery for renal tumors. Urology, 58: 688, 2001 14. Ward, J. P.: Determination of the Optimum temperature for regional renal hypothermia during temporary renal ischaemia. Br J Urol, 47: 17, 1975 15. Ackermann, D., Lenzin, A. and Tscholl, R.: Renal hypothermia in situ. Comparison between surface and perfusion cooling concerning renal function in pigs. Urologe A, 18: 38, 1979 16. Marberger, M., Georgi, M., Guenther, R. and Hohenfellner, R.: Simultaneous balloon occlusion of the renal artery and hypothermic perfusion in in situ surgery of the kidney. J Urol, 119: 463, 1978 17. Novick, A. C.: Surgery of the kidney. In: Campbell’s Urology, 8th ed. Edited by P. C. Walsh, A. B. Retik, E. D. Vaughan, Jr. and A. J. Wein. Philadelphia: W. B. Saunders Co., chapt. 12, p. 3570, 2002 18. Wagenknecht, L. V., Hupe, W., Bucheler, E. and Klosterhalfen, H.: Selective hypothermic perfusion of the kidney for intrarenal surgery. Eur Urol, 3: 62, 1977 19. Morishita, K., Yokoyama, H., Inoue, S., Koshino, T., Tamiya, Y. and Abe, T.: Selective visceral and renal perfusion in thoracoabdominal aneurysm repair. Eur J Cardiothorac Surg, 15: 502, 1999
Vol. 171, 68 –71, January 2004 Printed in U.S.A.
DOI: 10.1097/01.ju.0000101040.13244.c4
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA: RENAL ARTERY PERFUSION ¨ NTER JANETSCHEK,* ALAA ABDELMAKSOUD, FARIBORZ BAGHERI, HASSAN AL-ZAHRANI, GU KARL LEEB AND MANFRED GSCHWENDTNER From the Departments of Urology and Radiology (MG), Elisabethinen Hospital, Linz, Austria
ABSTRACT
Purpose: Laparoscopic partial nephrectomy represents a feasible option for patients with small renal masses. We describe our initial experience with laparoscopic partial nephrectomy in cold ischemia achieved by renal artery perfusion. Materials and Methods: From November 2001 to March 2003 laparoscopic partial nephrectomy in cold ischemia was performed in 15 patients with renal cell carcinoma. Cold ischemia was achieved by continuous perfusion of Ringers lactate at 4C through the renal artery, which was clamped. Tumor excision was performed in a bloodless field with biopsy taken from the tumor bed. The collecting system was repaired if needed. Renal reconstruction was performed by suturing over hemostatic bolsters. Results: All procedures were successfully completed laparoscopically by our new technique. Mean operative time was 185 minutes (range 135 to 220). Mean ischemia time was 40 minutes (range 27 to 101). Estimated mean intraoperative blood loss was 160 ml (range 30 to 650). Entry to the collecting system in 6 patients was repaired intraoperatively. Additional vascular repair was done in 2 patients. There were no significant postoperative complications. Postoperative followup in 8 patients showed that the renal parenchyma was not damaged by the ischemic period. Conclusions: Our initial experience of incorporating cold ischemia via arterial perfusion into laparoscopic partial nephrectomy shows the feasibility and safety of the technique. We believe that this approach has the potential to make laparoscopic partial nephrectomy for renal cell carcinoma safe and reliable. KEY WORDS: kidney; nephrectomy; laparoscopy; carcinoma, renal cell; renal artery
offers the surgeon extra time and, therefore, it has become the standard procedure during open surgery. To achieve results comparable to those of open surgery cold ischemia had to be integrated into laparoscopy. The feasibility of laparoscopic renal surface hypothermia by applying ice slush and renal hypothermia by retrograde ureteral cold saline perfusion, respectively, was already reported by others.11, 12 We present our first experience with renal cooling during laparoscopic surgery for small RCCs by cold arterial perfusion.
Within a short period laparoscopic radical nephrectomy for renal cell carcinoma (RCC) has become a standard of care.1 However, because of the widespread use of imaging techniques such as ultrasonography and computerized tomography (CT), a large number of small, localized renal tumors is detected incidentally.2 For such patients organ sparing surgery must be considered as an alternative to radical nephrectomy even if the contralateral kidney functions normally.3 Due to encouraging reports about tumor recurrence and cancer specific survival in cases of nephron sparing surgery (NSS), it is not unlikely that partial nephrectomy may become more frequent than radical nephrectomy in the future.3, 4 In 1993 the first laparoscopic partial nephrectomy in a porcine model was reported.5 At many centers groups have since developed their techniques to perform NSS by laparoscopy.6 – 8 We have previously described a technique to perform wedge resection for RCC by laparoscopy.9 However, this technique was restricted to tumors 2 cm or less since it was performed without inducing renal ischemia. To duplicate all principles of open surgery by laparoscopy we changed our technique by introducing renal ischemia and suture repair of the collecting system and renal parenchyma, as described by Gill et al.10 So-called warm ischemia is achieved by temporary occlusion of the renal artery alone or the artery and vein together. The time available to do partial resection and repair the collecting system and parenchyma during warm ischemia is limited and the surgeon must race against the clock. Renal cooling during ischemia protects the kidney,
MATERIALS AND METHODS
From November 2001 to March 2003 laparoscopic partial nephrectomy under cold ischemia was performed in 15 patients. During this period only 3 partial resections were performed without cooling the kidney and no open NSS was done. Table 1 lists patient demographics. The indication was suspected RCC with a mean tumor size of 2.7 cm (range 1.5 to 4). The indication was elective in 14 patients. In 1 patient with bilateral RCC the smaller tumor was removed by wedge resection and laparoscopic contralateral nephrectomy was performed 8 weeks later. Table 2 shows tumor locations. Four tumors were completely intrarenal, including 2 confined within the lower pole and 2 that were central. Metastatic evaluation was negative and all tumors were clinically T1, N0, M0. In all patients preoperative angiomagnetic resonance imaging was performed to assess the number and location of the renal arteries. Preoperative renal scintigraphy (mercaptoacetyltriglycine clearance for split renal function) was done to obtain baseline data on renal function for followup. Informed consent was obtained for the possibility of conversion to laparoscopic radical or open partial nephrectomy.
Accepted for publication August 22, 2003. * Correspondence: Department of Urology, Elisabethinen Hospital, A-4010 Linz, Postfach 239, Fadinger Strasse 1Austria (telephone: ⫹43-732-7676-4555; FAX: ⫹43-732-7676-4556; e-mail: [email protected]). 68
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA TABLE 1. Patient demographic Features Total No. pts No. men/women Mean age (range) Mean kg body wt (range) Mean mg/dl preop. serum creatinine (range) No. lesion side (%): Lt Rt
15 9/6 58 (36–76) 85.4 (57–130) 1.1 (0.91–1.30) 11 (73) 4 (27)
TABLE 2. Tumor location
Anterior Posterior Lat Medial
No. Upper Pole (side)
No. Middle Third (side)
No. Lower Pole (side)
1 (lt)
1 (rt) 1 (lt) 1 (lt) 3 (lt)
1 (lt) 4 (lt) 1 (rt)
2 (rt)
Technique. Preoperative preparation and anesthesia induction were done as usual. Placement of an open tip ureteral catheter, usually a single pigtail catheter, was done under fluoroscopy to be used later to determine collecting system integrity. An angiocatheter was then passed into the main renal artery through a femoral puncture on the ipsilateral side. To avoid dislodging the catheter this procedure was done by an interventional radiologist in the theater with the patient on the operating table. The patient was then brought to the 45-degree lateral decubitus position. In this final position for laparoscopic surgery the angiocatheter was again assessed and advanced in the renal artery close to the origin of the segmental arteries if needed. The approach to the kidney was transperitoneal in 14 patients and retroperitoneal in 1. Port placement varied according to tumor location. In addition to the 4 trocars usually required for radical nephrectomy, that is for the camera a 10 mm, for the right and left surgeon hands a 5 and a 10 mm, and for the retractor a 10 mm trocar, an additional 10 mm trocar for the tourniquet was placed in the lower abdomen. The thermoprobe was introduced through the sheeth of a Veress needle. The number of trocars was the same for the transperitoneal approach and retroperitoneoscopy. In the first 2 patients the renal hilum was not dissected and the renal artery was occluded by a balloon integrated into the angiocatheter. However, since some arterial bleeding occurred in the second patient, we preferred to use a tourniquet for artery occlusion in the following 13, which proved to be much safer. Therefore, an angiocatheter without a balloon was used. The renal artery was secured and later occluded using a tourniquet of 5 mm umbilical tape and a 10Fr silicone tube, which was placed as close to the origin of the artery as possible. We were prepared to occlude additional smaller arteries with laparoscopic bulldog clamps but it has not been required to date. Initially the renal vein was secured medial to the gonadal, lumbar and adrenal veins but not occluded in 11 patients, also using umbilical tape. However, we stopped securing the renal vein since there was no venous backflow due to the positive pressure of perfusate in the vein. Intravenous infusion of 200 cc 20% mannitol was given 15 minutes before arterial occlusion. After approaching the tumor the overlying fat was dissected and the renal capsule around the tumor was incised using a monopolar hook. Cold ischemia was then started. It was achieved by occluding the renal artery and perfusing 1,000 ml iced Ringers lactate at 4C at a rate of 50 ml per minute through the angiocatheter. Surgery was started immediately following the initiation of cold perfusion. Because of availability, 3 Infusomat fm (Braun, Meldungen, Germany) perfusion pumps were used simultaneously to achieve the required perfusion rate. Mannitol (100 ml 20%) was added to each 1,000 ml Ringers
69
lactate to achieve an osmolality of 430 mOsm/ml to avoid parenchymal edema.11 Renal temperature was continuously monitored with a thermocouple probe residing in the parenchyma. When a parenchymal temperature of 25C was attained, perfusion was decreased to maintain a steady state. The patient was warmed with a Bair Hugger (Augustine Medical Inc. Eden Prairie) warm air blanket and the temperature was continuously monitored by a thermocouple probe residing in the nasopharynx. Tumor excision was performed in a blood-free field using scissors but no diathermy (fig. 1). Biopsy was taken from the tumor bed. The tumor and overlying fat were placed in separate organ bags, which were removed later. The integrity of the collecting system was evaluated by injecting methylene blue through the pre-placed ureteral catheter. Occasionally injured large vessels in the tumor bed were clearly observed by a jet of perfusate. Therefore, the collecting system and injured vessels could be precisely repaired by figure-of-8 sutures using 4-zero polyglactin on a 17 mm 1/2 C needle (figs. 2 and 3). The cut edges of the parenchyma were approximated by 2 or 3 figure-of-8 sutures over a TapoTamb (Ethicon Sarl, Neuchatel, Switzerland) hemostatic bolster using zero polyglactin on a 36.4 mm needle (fig. 4). Fibrin glue (Baxter AG, Vienna, Austria) or a strip of a Tachocomb (Nycomed, Linz, Austria) was applied on the cut surface to avoid delayed bleeding. A tube drain was always left in place. Renal artery perfusion was terminated after the parenchymal sutures were tied. The renal artery catheter was removed following laparoscopic surgery. The arteriotomy was closed by a Perclose A-T (Abbott Vascular, Redwood City, California) percutaneous suture device. The urethral and ureteral catheters were removed on postoperative day 2 but they could be removed earlier if preferred. CT and renal scans were repeated 3 months postoperatively to document complete tumor removal, the integrity of repair and kidney function. RESULTS
Preoperative assessment of the arteries by angio-magnetic resonance imaging was always correct. Wedge resection was performed in 11 patients, major transverse resection was done in 2 and partial nephrectomy for central tumors was done in another 2 (figs. 1 and 3). These procedures were successfully terminated without conversion. Tourniquet placement was always possible without any problem. Tumor location was more important in regard to technical difficulty than the involved side. However, dissection of the right renal artery had to be performed in the interaortocaval space because of early artery
FIG. 1. Major transverse resection of lower right kidney pole
70
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA
FIG. 2. Left kidney. A, entry to collecting system is evidenced by methylene blue leakage. B, suture repair of collecting system with jet of perfusate issuing from cut vessel on tumor bed.
FIG. 3. Suture repair of left kidney (K) renal vein (V) in complete bloodless field after resection of centrally located tumor. R, renal parenchyma resection margin.
minutes. In 2 patients the thermocouple probe was dislodged during surgery. Mean laparoscopic operative time was 185 minutes (range 135 to 220). Ten to 20 minutes (mean 16) must be added for angiocatheter placement. Mean total ischemia time was 40 minutes (range 27 min to 101). The mean amount of perfusate was 1,580 ml (range 1,150 to 2,800). The mean decrease in body temperature during cold perfusion was 0.64C (range 0.5 to 1.1). Mean intraoperative blood loss was 160 ml (range 30 to 650). In 2 patients we noted high blood loss, which was due to insufficient balloon occlusion in 1 and intermittent perfusion pump failure in 1, which resulted in venous backflow from the injured renal vein. Only 1 patient required intraoperative blood transfusion. In another patient continuous flow of blood through the drain was observed postoperatively. Hemoglobin and hematocrit decreased to 9.9 gm/dl and 29.3%, respectively. Therefore, second look laparoscopy was performed on postoperative day 1. A suture had torn through the parenchyma. Surprisingly only little bleeding was observed at the operative site. The defect was covered by stripes of Tachocomb (Nycomed, Linz, Austria). Entry to the collecting system in 6 patients was repaired intraoperatively (fig. 2). Repair of the renal vein, segmental vein and artery was done in 2 patients in whom the tumors were located centrally, close to the hilum (fig. 3). Drainage was removed when its output was less than 50 ml per 24 hours. Mean hospital stay was 9.4 days (range 7 to 14). No urinary fistula or urinoma was observed. No postoperative morbidity due to puncture of the femoral artery or to the amount of perfusate was observed. Histopathological examination revealed RCC in 13 patients and angiomyolipoma in 2. Resection margins were negative in 14 patients. In 1 case a negative margin was not described where the tumor was in direct contact with the renal vein. During resection the vein was entered and repaired (fig. 3). To date postoperative renal function was evaluated in 8 patients. In 5 patients the decrease in renal function was 1%, 1%, 2%, 3% and 8%, respectively, on renal scintigraphy. In 3 patients followed elsewhere CT showed undisturbed perfusion of the renal parenchyma.
FIG. 4. Left kidney after complete parenchymal repair with sutures over hemostatic bolster.
DISCUSSION
branching. Angiocatheter dislodgment during dissection never occurred. Surgery was started immediately following the initiation of cold perfusion. It required about 10 minutes for the parenchymal temperature to decrease to 25C. To maintain the steady state of 25C the perfusion rate was decreased from 50 to 25 to 33 ml per minute. In 1 patient perfusion was inadequate because the catheter tip was not advanced beyond the tourniquet. However, in this patient total ischemia time was only 32
Laparoscopic NSS without renal ischemia is feasible and it can be achieved by step-by-step resection and hemostasis.9, 13 However, this technique has its drawbacks. It is restricted to tumors 2 cm or less in a favorable peripheral location and hemostasis is slow and tedious. Since the cut surface is continuously covered with blood and burned by extensive monopolar and bipolar coagulation, the distinction between tumor and normal renal tissue becomes difficult. It may compromise complete tumor resection. Necrotic urinary fistula due to diathermy close to the collecting system has been
LAPAROSCOPIC PARTIAL NEPHRECTOMY IN COLD ISCHEMIA
described.13 These reasons were why we replaced this technique with partial nephrectomy under cold ischemia. During ischemia the tissue is cut sharply in a blood-free field, avoiding diathermy. Normal renal tissue and tumor can be distinguished precisely, so that complete tumor resection can be continuously monitored. As in open surgery, hemostasis relies on suturing the cut edges of the parenchyma on bolsters of hemostatic material.10 A major restriction of this technique is time because renal damage is expected if ischemia time is longer than 30 minutes. Therefore, cooling the kidney, as in open surgery, is required if ischemia time is anticipated to be more than 30 minutes, as for larger tumors and tumors at unfavorable sites. In addition, unexpected problems during surgery may extend the operative time. The optimum temperature for hypothermic preservation is 15C, based on the canine experiments of Ward.14 A temperature of 20 to 25C is easier to maintain. Animal15 and human16, 17 studies have shown that this level of hypothermia provides complete renal protection from ischemia for at least 90 minutes. In situ renal hypothermia can be achieved with external surface cooling or perfusion of the kidney. These 2 methods are equally effective.15, 18, 19 The feasibility of surface cooling with ice slush by laparoscopy was reported recently.11 We chose the other alternative, namely arterial perfusion, because with this technique the laparoscopic part of the operation does not differ much from partial nephrectomy in warm ischemia. All necessary maneuvers are performed prior to surgery, so that the laparoscopic procedure is not rendered more complicated. Another innovative alternative was recently described. In 1 patient renal hypothermia was achieved by cold saline perfusion via the collecting system and a renal cortical temperature of 24C was achieved.12 Cold arterial perfusion has several advantages. A renal parenchymal temperature of 25C can be achieved rapidly. Therefore, tumor resection and parenchymal repair can be done at leisure in a clear, blood-free field. Due to positive perfusate pressure within the collecting system no venous backflow occurs. Continuous leakage and sometime even jets of perfusate do not disturb exposure, but rather allow us to identify cut and injured arterial and venous vessels in a completely blood-free field. In 2 complicated, centrally located tumors vascular lesions had to be repaired after removing the tumor, which was greatly facilitated by this effect. The use of a tourniquet to occlude the renal artery is probably mandatory to avoid an intimal lesion. However, we believe that a tourniquet is safer than a vascular clamp since it does not slide off and the artery can be re-occluded at any time in case of an emergency due to inadvertent bleeding. Damage to the renal parenchyma due to ischemia was not observed in any patient. However, there are several potential drawbacks to the method. Additional administration of intravenous fluids during surgery must be minimized to avoid fluid overload. Therefore, diuresis was induced directly after ischemia and no cardiopulmonary problems occurred. One should be aware of this specific risk in a solitary kidney, where fluid overload could theoretically be avoided by perfusate drainage through the cut left gonadal vein or venotomy. Dislodging the arterial catheter has been described.16 We never experienced this problem since the angiocatheter was introduced in the theater at the operating table and the catheter tip was advanced as far as possible. In this series we did not note a kidney with 2 or more arteries, compromising cooling. However, we were prepared to cannulate 2 arteries of equal size or perfuse the largest artery, while occluding the others with bulldog clamps. The cost factor may be a problem, according to the health system. Costs are increased since a radiologist is required in the theater and operative time is increased by about 20 minutes. In experienced hands the majority of laparoscopic partial nephrectomies can be performed in warm ischemia within 30 minutes. However, if an unexpected problem arises, irreversible
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function of the kidney is at risk. Cold ischemia by whatever method decreases this risk and allows the less skilled laparoscopist to perform this type of surgery. In addition, the scope of indications is increased for the experienced laparoscopist. CONCLUSIONS
Our initial experience with incorporating cold ischemia via arterial perfusion into laparoscopic partial nephrectomy shows the feasibility and efficacy of this technique. This approach allows the duplication of the principles of the open surgery and makes laparoscopic NSS for RCC safe and reliable. It also facilitates vascular repair during surgery for difficult central tumors. REFERENCES
1. Chan, D. Y., Cadeddu, J. A., Jarrett, T. W., Marshall, F. F. and Kavoussi, L. R.: Laparoscopic radical nephrectomy: cancer control for renal cell carcinoma. J Urol, 166: 2095, 2001 2. Lightfood, N., Conlon, M., Kreiger, N., Bissett, R., Desai, M., Warde, P. et al: Impact of noninvasive imaging on increased incidental detection of renal cell carcinoma. Eur Urol, 37: 521, 2000 3. Herr, H. W.: Partial nephrectomy for unilateral renal cell carcinoma and a normal contralateral kidney: 10-year followup. J Urol, 161: 33, 1999 4. Fergany, A. F., Hafez, K. S. and Novick, A. C.: Long-term results of nephron sparing surgery for localized renal cell carcinoma: 10-year followup. J Urol, 163: 442, 2000 5. McDougall, E. M., Clayman, R. V., Chandhoke, P. S., Kerbl, K., Stone, A. M., Wick, M. R. et al: Laparoscopic partial nephrectomy in the pig model. J Urol, 149: 1633, 1993 6. Winfield, H. N., Donovan, J. F., Lund, G. O., Kreder, K. J., Stanley, K. E., Brown, B. P. et al: Laparoscopic partial nephrectomy: initial experience and comparison to the open surgical approach. J Urol, 153: 1409, 1995 7. Rassweiler, J. J., Abbou, C., Janetschek, G. and Jeschke, K.: Laparoscopic partial nephrectomy. The European experience. Urol Clin North Am, 27: 721, 2000 8. McDougal, E. M., Elbahnasy, A. M. and Clayman, R. V.: Laparoscopic wedge resection and partial nephrectomy—the Washington University experience and review of the literature. JSLS, 2: 15, 1998 9. Janetschek, G., Daffner, P., Peschel, R. and Bartsch, G.: Laparoscopic nephron sparing surgery for small renal cell carcinoma. J Urol, 159: 1152, 1998 10. Gill, I. S., Desai, M. M., Kaouk, J. H., Meraney, A. M., Murphy, D. P., Sung, G. T. et al: Laparoscopic partial nephrectomy for renal tumor: duplicating open surgical techniques. J Urol, 167: 469, 2002 11. Abreu, S. C., Gill, I. S., Ng, C., Mihir, D., Steinberg, A., Ramani, A. et al: Technique of laparoscopic renal hypothermia for partial nephrectomy. J Urol, suppl., 169: 20, abstract V77, 2003 12. Landman, J., Venkatesh, R., Lee, D., Vanlangendonck, R., Morissey, K., Andriole, G. L. et al: Renal hypothermia achieved by retrograde endoscopic cold saline perfusion: technique and initial clinical application. Urology, 61: 1023, 2003 13. Jeschke, K., Peschel, R., Wakonig, J., Schellander, L., Bartsch, G. and Henning, K.: Laparoscopic nephron-sparing surgery for renal tumors. Urology, 58: 688, 2001 14. Ward, J. P.: Determination of the Optimum temperature for regional renal hypothermia during temporary renal ischaemia. Br J Urol, 47: 17, 1975 15. Ackermann, D., Lenzin, A. and Tscholl, R.: Renal hypothermia in situ. Comparison between surface and perfusion cooling concerning renal function in pigs. Urologe A, 18: 38, 1979 16. Marberger, M., Georgi, M., Guenther, R. and Hohenfellner, R.: Simultaneous balloon occlusion of the renal artery and hypothermic perfusion in in situ surgery of the kidney. J Urol, 119: 463, 1978 17. Novick, A. C.: Surgery of the kidney. In: Campbell’s Urology, 8th ed. Edited by P. C. Walsh, A. B. Retik, E. D. Vaughan, Jr. and A. J. Wein. Philadelphia: W. B. Saunders Co., chapt. 12, p. 3570, 2002 18. Wagenknecht, L. V., Hupe, W., Bucheler, E. and Klosterhalfen, H.: Selective hypothermic perfusion of the kidney for intrarenal surgery. Eur Urol, 3: 62, 1977 19. Morishita, K., Yokoyama, H., Inoue, S., Koshino, T., Tamiya, Y. and Abe, T.: Selective visceral and renal perfusion in thoracoabdominal aneurysm repair. Eur J Cardiothorac Surg, 15: 502, 1999