Laparoscopic Partial Nephrectomy: Ready for Prime Time

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1 available at journal homepage: Laparoscopic Partial Nephrectomy: Ready for Prime Time Monish Aron, Georges-Pascal Haber, Inderbir S. Gill * Section of Laparoscopic and Robotic Surgery, Glickman Urological Institute, Cleveland Clinic Foundation, Cleveland, OH 44195, United States Article info Keywords: Kidney Laparoscopic partial nephrectomy Renal Tumour Please visit europeanurology to read and answer questions on-line. The EU-ACME credits will then be attributed automatically. Abstract Objectives: To review the development, techniques, outcomes, and current status of laparoscopic partial nephrectomy (LPN) for renal tumours. Methods: A Medline search ( ) was performed using the following keywords: kidney, laparoscopic partial nephrectomy, renal, and tumour. Over 300 papers were identified. Of these, 47 papers were selected for review based on their contribution to evolution of concepts, development of techniques, and perioperative and oncologic outcomes after LPN. Results: LPN provides perioperative results as well as intermediate and long-term oncologic and functional outcomes comparable to the reference standard (open partial nephrectomy [OPN]) with significantly decreased patient morbidity. The 5-yr oncologic data are available for 50 patients, with a mean tumour size of 3 cm (range cm). Renal cell carcinoma (RCC) was confirmed in 64% with tumour stage pt1a in 91%. At a median follow-up of 5.2 yr, overall and cancer-specific survival rates were 84% and 100%, respectively. Conclusions: As global experience and skills with this technique increase, the number of patients undergoing this procedure is increasing rapidly. In expert hands, cancer control and functional outcomes are comparable to OPN. # 2006 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Section of Laparoscopic and Robotic Surgery, Glickman Urological Institute, Cleveland Clinic Foundation, Cleveland, OH 44195, United States. Tel ; Fax: address: gilli@ccf.org (I.S. Gill). 1. Introduction Incidentally diagnosed small (4 cm) renal masses are currently the most commonly encountered renal tumours in urologic practice [1]. Open partial nephrectomy (OPN) is often regarded as the reference standard for the surgical treatment of the small renal mass. Although OPN provides excellent oncologic and functional outcomes, the morbidity of the flank incision is real and considerable [2]. Several minimally invasive nephron-sparing surgery (MINSS) options are available for select patients with small renal masses. These include extirpative (laparoscopic partial nephrectomy [LPN]) as well as ablative procedures. LPN is technically challenging and requires advanced, time-sensitive laparoscopic skills [3]. Potential benefits of LPN are decreased morbidity, shorter hospital stays and convalescence, and preservation of renal function, while providing cancer /$ see front matter # 2006 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eursup

2 969 control and functional outcomes comparable to OPN. To review the development, techniques, outcomes, and current status of LPN, we performed a Medline search ( ) using the following keywords: kidney; laparoscopic partial nephrectomy; renal; and tumour. More than 300 papers were identified. Of these; 47 papers were selected for review based on their contribution to evolution of concepts; development of techniques; and perioperative; functional; and oncologic outcomes after LPN. 2. Pertinent concepts of NSS Renal cell carcinoma (RCC) accounts for nearly 3% of all adult malignancies. Overall, 7 25% of RCC may be multifocal, and for tumours 4 cm the incidence of multifocality is 0 5%. Local recurrence after NSS is seen in <10% and could be attributed to undetected microscopic RCC in the renal remnant. However, no predictable relationship between multifocality and local recurrence has been reported [4]. To prevent local recurrence, tumour excision with a margin of surrounding normal parenchyma is essential. The primary goal is a negative margin, with margin width having no clinical consequence [5]. During LPN a margin of approximately 0.5 cm is desired to prevent tumour spill. Small renal tumours usually have a slow rate of growth and hence could take several years to become a significant threat to the patient. Therefore, in elderly and infirm patients with significant associated comorbidity, a policy of watchful waiting may be a viable option. If active intervention is indicated, OPN is the reference standard for the treatment of the renal mass <4 cm. For such tumours, the 5- and 10-yr cancer cure rates are comparable to those for radical nephrectomy [6,7]. LPN is a minimally invasive alternative to the reference standard. It is imperative that oncologic principles not be compromised and hence laparoscopic surgeons must endeavour to duplicate techniques of OPN during LPN. In addition, prospective accrual of perioperative and 5-yr oncologic data are of critical importance. 3. Indications and contraindications for LPN Absolute indications include synchronous bilateral RCC, tumour in a solitary kidney, or unilateral tumour with a poorly or nonfunctioning contralateral kidney, wherein radical nephrectomy would render the patient anephric. Five and 10-yr cancerspecific survival rates of 81% and 64% have been reported after open NSS in a solitary kidney and are a testimony to its safety and applicability in this scenario [8]. Relative indications exist where the contralateral kidney is at risk for future compromise: hereditary RCC, genetic diseases with risk of metachronous kidney cancer, diabetes, hypertension, stone disease, or renovascular disease. Elective indications for partial nephrectomy comprise renal tumours 4 cm or indeterminate cysts with malignant potential in the presence of a normal contralateral kidney. Novick [9] reported results of elective OPN for localised RCC in 315 patients. With a tumour size <3.5 cm, a cancer-specific survival rate of 95% and local recurrence in only two patients with approximately 3 yr of follow-up were reported. Herr [10] reported a 97% 10-yr cancer-free survival after elective NSS for tumours with a mean size of 3 cm in the presence of a normal contralateral kidney. Increasing experience and advances in laparoscopic techniques have led to refinements in renal hilar control, tumour excision, pelvicaliceal repair, and haemostatic reconstruction of the parenchymal defect [3,11]. Clinical LPN was first performed transperitoneally by Winfield et al. [12] and retroperitoneally by Gill et al. [13]. LPN was initially limited to the treatment of select exophytic, small, and peripheral tumours [14,15]. With increasing experience, these indications have been extended to include tumours infiltrating well into the renal sinus, completely intrarenal tumours, hilar tumours, tumours in a solitary kidney, large tumours, and tumours in the presence of renovascular disease [16 20]. Current contraindications for LPN include a completely central intrarenal tumour, tumours with a caval thrombus, and prior open kidney surgery. Morbid obesity and the presence of more than two tumours increase the technical difficulty of LPN. Patients with a coagulopathy and platelet dysfunction must be approached with caution. 4. Techniques The technical issues during LPN are achieving a bloodless field for tumour excision, repair of the collecting system, haemostasis, and reconstruction of the parenchymal defect in a time-sensitive manner, while minimising compromise of renal function.

3 Bloodless field and haemostasis Currently, the only established and safe method of obtaining a near bloodless field during LPN is to clamp the renal hilum. Modalities of hilar control include clamping the artery alone or both artery and vein, or using intermittent clamping. Advantages and disadvantages of these methods are debatable. Our preference is to clamp both the artery and the vein for the duration of the tumour excision and reconstruction of the defect. Various methods have been used to achieve haemostasis. Suture ligation of divided blood vessels and a sutured renorrhaphy over haemostatic material are used during OPN; these are the methods we replicate in our practice. Admittedly, these are advanced laparoscopic suturing maneuvers that require advanced skills and experience. Alternatives such as radiofrequency (RF) coagulation [21] and application of thrombin gel slurry [22] have been used as haemostatic tools during LPN. A monopolar RF device that achieves dissection and haemostasis has recently been reported for unclamped LPN in 10 patients with a mean tumour size of 3.9 cm [23]. The haemostatic agent FloSeal 1 (Baxter Healthcare, Deerfield, IL) was evaluated at our institution where patients undergoing LPN with FloSeal were compared with patients who underwent LPN without FloSeal [24]. The FloSeal group had a lower rate of haemorrhagic complications (12% vs. 3%) Warm ischaemia Critical renal warm ischaemia (WI) time has generally been considered to be 30 min. LPN may require longer WI times compared to OPN [25]. Recent evidence suggests that WI time >30 min during LPN may not significantly worsen renal function after LPN [26]. Laven et al. reported their experience with prolonged WI in a solitary kidney porcine model [27]. At 15 d after the procedure, they found no significant decrease in glomerular filtration rate or increase in serum creatinine concentration even after 90 min of WI. Additionally, no differences in functional outcomes were found between the animals treated with open surgery versus those treated laparoscopically. Shekarriz et al. [28] reported the effect of WI on renal function after LPN in 17 patients. Mean WI time was 22.5 min (range: min) and did not correlate with change in renal function. Desai et al. [29] evaluated the impact of WI on renal function in 179 patients with special emphasis on 15 with a solitary kidney. In patients with a solitary kidney, the mean WI time was 29 min, amount of parenchyma excised was 29%, and the serum creatinine level at baseline and mean follow-up of 4.8 mo was 1.3 and 1.8 mg/dl, respectively Renal cooling Various techniques of renal cooling during LPN are reported. Gill et al. reported a technique of intracorporeal surface hypothermia in 12 patients [30]. The kidney was mobilised in situ and an Endo-catch II bag (US Surgical, Norwalk, CT) was placed around it. The hilum was occluded with a vascular clamp, the bottom of the bag retrieved through a port site, and ice-slush rapidly delivered into the bag to achieve core renal temperatures of C. Continuous perfusion of a crystalloid solution at 4 8C through an angiocatheter in the clamped renal artery to maintain a parenchymal temperature of 25 8C was reported by Janetschek et al. [31]. Cortical and medullary temperatures of 24 8C and 21 8C, respectively, have also been achieved by retrograde pelvicaliceal cold saline perfusion via a ureteral access sheath [32]. A technique to cool the kidneys to C during LPN in a porcine model using fine ice slush delivered through a 10-mm laparoscopic endeffector has also been reported [33] Collecting system repair Our practice is to routinely check for pelvicaliceal entry using a retrograde injection through a preplaced ureteral catheter. If such entry is identified, we suture it in a watertight fashion. We routinely use a ureteral catheter because it allows precise identification of the site of pelvicaliceal entry and allows testing the watertightness of pelvicaliceal system repair. Desai et al. [11] compared the perioperative data of 27 LPNs with pelvicaliceal entry with 37 LPNs with no pelvicaliceal entry. Pelvicaliceal suture repair was associated with longer hospital stay and longer WI time. No patient undergoing pelvicaliceal repair developed urinary leak Cleveland Clinic technique Our current technique of LPN has been reported earlier [34]. Briefly, a retrograde 5F ureteral catheter is placed in the renal pelvis for intraoperative injection of dilute methylene blue. The patient is placed in a 608 flank position for the transperitoneal approach and the 908 lateral position for the retroperitoneal approach. The hilum is identified initially. For the retroperitoneal procedure the artery and vein are circumferentially mobilised separately.

4 971 For the transperitoneal approach space is created all around the hilum for application of the Satinsky clamp, but the vessels are not individually mobilised. The kidney is strategically defatted maintaining perirenal fat over the tumour. Intraoperative ultrasound is performed to mark the tumour limits with an adequate margin of normal parenchyma. The hilum is clamped en bloc with the Satinsky clamp for the transperitoneal procedure and with bulldog clamps for the retroperitoneal procedure. Intravenous mannitol is given (12.5 g) min prior to hilar clamping. The tumour and overlying fat are excised with cold Endoshears in a nearbloodless field. The collecting system is suture repaired with a running 2-0 Vicryl suture. Watertightness of the caliceal repair is confirmed by repeat retrograde injection. Renorrhaphy is performed with three to six interrupted sutures of 1-0 Vicryl over a pre-prepared Surgicel bolster (Johnson & Johnson, New Brunswick, NJ). A Hem-o-Lok 1 clip (Weck Closure System, Research Triangle Park, NC) is secured on the suture to prevent it from pulling through. FloSeal is applied to the cut parenchymal surface underneath the bolster. Another Hem-o-Lok clip is applied to the suture flush with the opposite renal surface, compressing the kidney. The suture is then tightly tied across the bolster, maintaining adequate parenchymal compression. Mannitol (12.5 g) and furosemide (10 20 mg) are given intravenously and the hilum is unclamped. The abdomen is reinspected after 5 min of zero pneumoperitoneum to ensure good haemostasis. The specimen is removed in an Endo-catch bag and a drain is placed prior to exiting the abdomen. 5. Perioperative and oncologic data 5.1. Cleveland Clinic experience The senior author s personal experience with LPN exceeds 550 cases (personal communication). In the initial 5 yr ( ), we performed 91 LPNs for patients with mean age of 64 yr, mean body mass index (BMI) of 30 kg/m 2, and mean tumour size 2.9 cm; 35% of the patients had tumours 3 cm. An imperative indication for LPN was present in 30%. Renal insufficiency (serum creatinine >1.4 mg/dl) existed in 13%. From 2002 to 2005 we performed 408 LPNs with mean patient age of 58 yr, mean BMI of 29 kg/m 2, and mean tumour size 2.8 cm; 31% of patients had tumours >3 cm. Renal insufficiency existed in 9% and an imperative indication in 27%. Of 499 tumours, 55% were peripheral, 39% were central, and 6% were hilar, with tumours being anterior in 350 patients and posterior in 149. Final pathology was RCC in 75%. Perioperative parameters in the 408 patients ( ) revealed a mean operating (OR) time of 204 min, mean estimated blood loss (EBL) of 265 ml, mean WI time of 31.7 min, and hospital stay of 3.2 d. Intraoperative complications occurred in 7.8% and postoperative complications in 15%. Blood transfusion was required in 3%. Open conversion was needed in five patients (1.2%), including two (0.4%) for nephrectomy. In 100 patients with 3 yr of follow-up, positive margins were seen in 2 patients; however, no recurrence or metastases were noted. At a mean follow-up of 42 mo (range: mo), overall survival was 86% and cancer-specific survival was 100% [35]. The 5-yr data are now available for 50 patients treated at our institution; their mean tumour size was 3 cm (range: cm). Surgical margin was positive in one patient. RCC was confirmed in 64% with tumour stage pt1a in 91%. At a median follow-up of 5.2 yr, overall and cancerspecific survival rates were 84% and 100%, respectively [36]. In a multicenter European experience of 53 LPNs [37], the mean tumour size was 2.3 cm (range: 1 5 cm). Mean OR time was 191 min (range: min) and EBL 725 ml (range: ml). Operative complications included one patient with pneumothorax and four with bleeding, of whom two were converted. Two patients required subsequent nephrectomy. Histology showed 69% pt1 RCC and 100% cancer-specific survival at 3 yr. Jeschke et al. [38] reported LPN without hilar clamping in 51 patients with tumours <2 cm, using ultrasonic scalpel and bipolar coagulation with fibrin glue-coated cellulose. OR time was 132 min (range: min), EBL was 282 ml (range: ml), and no open conversion was necessary. Complications occurred in 10%. At a follow-up of 34 mo (range: 3 78 mo), neither local recurrence nor distant metastases occurred. Weld et al. [39] reported 60 LPNs without any conversion. RCC was documented in 60%, with no positive margins or recurrence at 25 mo. The overall complication rate was 30% (13%, urologic; 17%, nonurologic). Wille et al. [40] reported 44 LPNs for exophytic tumours with a median diameter of 3 cm (range: 1 5 cm), performed by three surgeons at one center. The hilum was clamped in 56%. Mean surgical time was 210 min (range: min) and WI time was 21 min (range: 7 41 min). Positive margins on frozen section were seen in 16%. At a mean follow-up of 15 mo (range: 6 37 mo), no recurrence was observed.

5 972 Abukora et al. [41] reported a 10-yr experience with LPN in 78 patients, including unclamped LPN in 29, and clamped LPN in 49 (cold ischaemia in 24 and WI in 25 patients). Three patients in the clamped group were converted to open surgery. At a mean follow-up of 24 and 12 mo for the clamped and unclamped groups, respectively, there were no recurrences Extending the indications for LPN Laparoscopic heminephrectomy (resection >30% of renal parenchyma) was reported in 41 patients and results compared to a group of 41 consecutive patients who underwent LPN with <30% resection [18]. The heminephrectomy group had larger tumours (3.7 vs. 2.3 cm) that were more often central (41% vs. 9.8%). WI time was longer for heminephrectomy (39 vs. 33 min); however EBL (150 vs. 100 ml) and OR time (220 vs. 190 min) were comparable. Our group compared LPN for central tumours (n = 154) with LPN for peripheral tumours (n = 209) [16]. Central tumours were larger (3 vs. 2.4 cm) than peripheral tumours and had longer operating time (210 vs. 180 min), WI time (33.5 vs min), and hospital stay (67 vs. 60 h). Early complications were more common in the central group (6% vs. 2%). Gill et al. [17] reported the outcomes of LPN for 25 patients with hilar tumours. Mean tumour size was 3.7 cm (range: cm); four patients (16%) had a solitary kidney. WI time was 36.4 min (range: min), EBL was 231 ml (range: ml), and OR time was 3.6 h (range; 2 5 h). Haemorrhagic complications occurred in three patients (12%). We [19] reported LPN for 22 patients with a tumour in a solitary kidney. Mean tumour size was 3.6 cm (range; cm), median EBL was 200 ml (range: ml), WI time was 29 min (range: min), OR time was 3.3 h (range: h), and hospital stay was 2.8 d (range: d). Two patients (9%) were converted to open surgery. Serum creatinine levels and glomerular filtration rates reflected a change of 33% and 27%, commensurate with the 23% parenchymal excision Complications In the first 200 LPNs at our institution, perioperative complications occurred in 66 patients (33%) [42]. Open conversion was required in two patients (1%). Reoperative laparotomy was necessary in four patients (2%). Overall, haemorrhagic complications occurred in 19 patients (9.5%). Urine leak occurred in nine patients (4.5%). Other urologic and nonurologic complications occurred in 4.5% and 15%, respectively. Our complication rates have decreased significantly since we started using FloSeal. When comparing LPN without FloSeal to LPN with FloSeal [24], the FloSeal group had decreased overall complications (37% vs. 16%), a lower rate of haemorrhagic complications (12% vs. 3%), and less urine leakage (6% vs. 1.5%) Comparison with OPN No prospective randomised comparison between LPN and OPN is available in the literature. Early in our LPN experience we compared our initial patients undergoing LPN (n = 100) with a mature experience of OPN (n = 100) for a solitary tumour 7 cm[25]. The median tumour size was 2.8 cm versus 3.3 cm. Median OR time (3 vs. 3.9 h; p < 0.001) and EBL (125 vs. 250 ml; p < 0.001) were lower in the LPN group, whereas WI time was longer during LPN (28 vs. 18 min). LPN patients required less analgesia (20 vs. 252 mg morphine; p < 0.001), had shorter hospital stays (2 vs. 5 d; p < 0.001), and had a quicker convalescence (4 vs. 6 wk; p < 0.001). Median preoperative serum creatinine (1.0 vs. 1.0 mg/dl; p = 0.52) and postoperative serum creatinine levels (1.1 vs. 1.2 mg/dl; p = 0.65) were similar in the two groups Cost factors In a cost comparison of nephron-sparing techniques, Lotan and Cadeddu [43] found that there was no significant difference in cost between LPN and OPN because the shorter stay with LPN compensated for the higher cost of disposables. 6. Potential directions for the future Further developments in the field are necessary to allow more surgeons to perform LPN. Safe methods of unclamped LPN and bloodless techniques for parenchymal incision need to be refined. Hydro-jet technology [44,45] uses a high-pressure water jet to perform selective tissue dissection in a relatively bloodless manner. Intrarenal vessels may then be controlled with clips or bipolar coagulation and the collecting system suture repaired. The feasibility and short-term outcomes of the 80-W potassiumtitanyl-phosphate (KTP) laser-unclamped LPN [46] have been reported in the survival calf model (6 calves, 12 kidneys). Parenchymal resection and haemostasis were achieved solely with the laser, without any additional sutures. All 12 procedures were successful, 11 (92%) without hilar clamping.

6 973 Limitations included considerable smoke generation during laser LPN and higher CO 2 inflow requirement. Until the time such unclamped resection becomes a reality, complex excisions and reconstructions may require some form of cooling of the kidney. Laparoscopic renal hypothermia is still evolving. A user-friendly method that reproducibly reduces renal temperature to 15 8C may extend the indications of LPN. Nearly 20 30% of all renal tumours that are subjected to NSS are actually benign on final histopathology. These patients could potentially avoid an operation and its associated morbidity if we had a consistent method to discriminate benign from malignant masses preoperatively. At this writing, no such completely reliable method exists. Whether a combination of thin-slice imaging and needle biopsy will provide such answers remains to be seen. There is also a need for an on-table determination of negative margins as soon as the tumour is excised. When in doubt, the conventional method is to send a frozen section biopsy from the tumour bed. If this biopsy is positive, one may need to take down the repair to extend the excision and also the WI time. Optical coherence tomography (OCT) has been shown to provide an optical biopsy of tissues in various non-urologic fields. However, its potential application in the setting of LPN is not currently clear. Other potential significant advances could possibly include methods of treatment that are truly noninvasive in nature. These could include highly refined and advanced needle-probe ablative techniques as well as radiosurgery [47]. Most such techniques are still either developmental or experimental. 7. Conclusions NSS is currently the preferred treatment for the small renal mass. OPN is the standard against which all other modalities of NSS need to be compared. LPN has come a long way in a span of 5 yr. The technique is becoming standardised and the procedure more prevalent at centers of excellence around the world. In the hands of experienced surgeons, the rates of haemorrhagic complications, positive margins, and urinary leakage are comparable to those of contemporary OPN series. Preliminary 5-yr data for LPN are just becoming available, and in skilled hands, LPN is certainly ready for prime time. References [1] Luciani LG, Cestari R, Tallarigo C. Incidental renal cell carcinoma-age and stage characterization and clinical implications: study of 1092 patients. Urology 2000;56: [2] Chatterjee S, Nam R, Fleshner N, Klotz L. Permanent flank bulge is a consequence of flank incision for radical nephrectomy in one half of patients. Urol Oncol 2004; 22:36 9. [3] Gill IS, Desai MM, Kaouk JH, et al. Laparoscopic partial nephrectomy for renal tumor: duplicating open surgical techniques. J Urol 2002;167: [4] Uzzo RG, Novick AC. Nephron sparing surgery for renal tumors: indications, techniques and outcomes. J Urol 2001;166:6 18. [5] Castilla EA, Liou LS, Abrahams NA, et al. Prognostic importance of resection margin width after nephronsparing surgery for renal cell carcinoma. Urology 2002; 60: [6] Fergany AF, Hafez KS, Novick AC. Long term results of nephron sparing surgery for localized renal cell carcinoma: 10-year follow-up. J Urol 2000;163: [7] Lee CT, Katz J, Shi W, Thaler HT, Reuter VE, Russo P. Surgical management of renal tumors 4 cm or less in a contemporary cohort. J Urol 2000;163: [8] Ghavamian R, Cheville JC, Lohse CM, Weaver AL, Zincke H, Blute ML. Renal cell carcinoma in the solitary kidney: an analysis of complications and outcome after nephron sparing surgery. J Urol 2002;168: [9] Novick AC. Partial nephrectomy for renal cell carcinoma. Urology 1995;46: [10] Herr HW. Partial nephrectomy for unilateral renal carcinoma and a normal contralateral kidney: 10-year followup. J Urol 1999;161:33 4. [11] Desai MM, Gill IS, Kaouk JH, Matin SF, Novick AC. Laparoscopic partial nephrectomy with suture repair of the pelvicaliceal system. Urology 2003;61: [12] Winfield HN, Donovan JF, Godet AS, Clayman RV. Laparoscopic partial nephrectomy: initial case report for benign disease. J Endourol 1993;7: [13] Gill IS, Delworth MG, Munch LC. Laparoscopic retroperitoneal partial nephrectomy. J Urol 1994;152: [14] McDougall EM, Elbahnasy AM, Clayman RV. Laparoscopic wedge resection and partial nephrectomy the Washington University experience and review of the literature. JSLS 1998;2: [15] Janetschek G, Jeschke K, Peschel R, Strohmeyer D, Henning K, Bartsch G. Laparoscopic surgery for stage T1 renal cell carcinoma: radical nephrectomy and wedge resection. Eur Urol 2000;38: [16] Frank I, Colombo Jr JR, Rubinstein M, Desai M, Kaouk J, Gill IS. Laparoscopic partial nephrectomy for centrally located renal tumors. J Urol 2006;175: [17] Gill IS, Colombo Jr JR, Frank I, Moinzadeh A, Kaouk J, Desai M. Laparoscopic partial nephrectomy for hilar tumors. J Urol 2005;174: [18] Finelli A, Gill IS, Desai MM, et al. Laparoscopic heminephrectomy for tumor. Urology 2005;65:473 8.

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