Inderbir S. Gill, Vice-Chairman, Glickman Urological Institute, Lerner College of Medicine, Section of Laparoscopic and Robotic Surgery, Cleveland Clinic Foundation, Cleveland, Ohio 44195, USA. e-mail: email@example.com
Epithelial tumours of the kidney account for ≈ 3% of all solid tumours and affect men nearly twice as often as women; ≈ 35 710 new cases of kidney cancer were expected to occur in the USA in 2004 . The incidence rate of kidney cancer has increased steadily over the last three decades, from of 7.1/100 000 in 1975 to 13/100 000 in 2003 . Between 1975 and 1995, the incidence of RCC increased annually by 2.3% among White men, 3.1% among White women, 3.9% among Black men and 4.3% among Black women . Similar increases in incidence were noted in 17 of 20 countries across four continents (Sweden, Denmark and Switzerland being exceptions) between 1973 and 1992 . The greatest increase in incidence was for localized tumours, although such trends were noted even for advanced tumours . Between 1986 and 1994, there was a 73% increase in the use of CT or MRI among Medicare beneficiaries, and this played a role in the earlier detection of pre-symptomatic renal tumours. However, the increased detection of incidental tumours does not completely explain the increasing trend in the incidence of renal tumours .
Despite this increase in incidence, the 5-year relative survival rates have improved from 52% in 1976, to 63% in 1999 . An incidentally diagnosed small renal mass is currently the most common renal tumour in urological practice . There has been a progressive increase in incidental tumours, from 13% in 1982 to 59% in 1997. Concomitantly, the mean size of the renal tumour has decreased from 6.8 cm in 1988 to 6 cm in 2002 . This trend has provoked the development and refinement of methods of treatment that aim to provide excellent cancer control with reduced morbidity.
To review the development, techniques, outcomes, and current status of laparoscopic partial nephrectomy (LPN) we searched Medline (1996–2006) using the keywords: ‘kidney’, ‘laparoscopic partial nephrectomy’, ‘renal’, and ‘tumour’; >350 papers were identified. Of these, selected reports were reviewed based on their contribution to the development of concepts, techniques, and peri-operative, functional and oncological outcomes after LPN.
RATIONALE FOR NEPHRON-SPARING SURGERY (NSS)
Despite recent developments in probe-based ablative therapies and availability of newer systemic therapy, surgical excision remains the cornerstone of treatment for RCC. Radical nephrectomy (RN), popularized by Robson et al. in the 1960s, remained the reference standard for surgical treatment of RCC for over two decades. Improvements in imaging and surgical technique over the last two decades led to the establishment of NSS as the preferred treatment for the small renal mass [8–16]. For such indications, PN has been shown to provide better functional outcomes and equivalent cancer control than RN . With a normal contralateral kidney, the cumulative incidence of renal insufficiency (defined as a serum creatinine level of ≥ 2.0 mg/dL) at 10 years was reported to be significantly higher after RN than after PN (22% vs 12%) . Proteinuria was also more common after RN (55% vs 35%) . Also, metachronous renal tumours in the contralateral kidney can occur in up to 10% of patients , underscoring the importance of avoiding unnecessary nephron loss.
RATIONALE FOR MINIMALLY INVASIVE NSS (MINSS)
Open PN (OPN) laid the foundations and became the reference standard for the surgical treatment of the small renal mass. OPN is associated with excellent oncological and renal functional outcomes. However, it is also associated with the morbidity of the muscle-cutting, open flank incision, which can be durable in up to half of patients . In addition, a substantial fraction of solid renal masses are benign. In a study of 2770 resections of solid renal tumours, 12.8% were found to be benign. When stratified by size, the proportion of benign masses was 25% for masses <3 cm, 30% for masses <2 cm, and 46% for masses <1 cm . Subjecting a patient with a one in three chance of having a benign tumour to a significantly morbid flank incision seems to be less than ideal. Such concerns and the clear need to decrease procedure-related morbidity have fuelled the significant advances in MINSS in the last 5 years.
Currently, two types of MINSS options are available: (a) excisional MINSS, i.e. LPN; and (b) ablative MINSS, i.e. cryoablation and radiofrequency (RF) ablation. At present, LPN provides functional and oncological outcomes comparable with OPN. Probe-based ablative techniques must still be considered developmental, as there are no long-term oncological data and no histological confirmation of complete cancer-cell death. Noninvasive ablative techniques such as radiosurgery and high-intensity focused ultrasound are still experimental.
DEVELOPMENT, INDICATIONS AND CONTRAINDICATIONS OF LPN
McDougall et al. first reported LPN in a pig model in 1993; clinical LPN was first reported transperitoneally in 1993 by Winfield et al. and retroperitoneally in 1994 by Gill et al.. Appropriately, LPN was initially limited to the treatment of small, exophytic, peripheral tumours. With increasing experience, these indications have been carefully and gradually expanded to include more technically challenging tumours: central tumours abutting the renal sinus, completely intrarenal tumours, hilar tumours, tumour in a solitary kidney, large tumours requiring heminephrectomy, ≥ pT2 tumours, multiple tumours, and tumours in the presence of concomitant renovascular disease [22–29].
Current indications for LPN parallel those for OPN at centres where such expertise is available (Table 1). Similar to OPN, at present most appropriately selected patients with an organ-confined renal mass of <4–7 cm are probably amenable to LPN. The primary contraindication to LPN is lack of surgeon experience and expertise with advanced laparoscopy. Other contraindications specific to LPN are infrequent, and include previous open kidney surgery, a small tumour with a renal vein thrombus (a situation that the present authors have not encountered), and a complex mid-pole completely intrarenal/hilar tumour in a patient with an absolute indication for NSS. Morbid obesity and two or more tumours increase the technical difficulty of LPN.
Table 1. The indications for LPN
Tumour in a solitary kidney
Unilateral tumour with poorly/non-functioning contralateral kidney
Relative (contralateral kidney at risk for future compromise)
Genetic diseases with risk of metachronous kidney cancer
Diabetes mellitus, hypertension, stone disease, or renovascular disease
Elective (normal contralateral kidney)
Renal tumour ≤ 4 cm
Indeterminate cyst with malignant potential
CHOICE OF APPROACH: TRANSPERITONEAL VS RETROPERITONEAL
The choice of laparoscopic approach is based on: (i) surgeon preference and training; (ii) tumour location; and (iii) tumour size. Essentially, our preference is to use the transperitoneal approach for most LPN cases, except for a posterior or posteromedial polar tumour (upper or lower pole), where we would elect to use the retroperitoneal approach. For a posterior interpolar tumour, we now prefer a transperitoneal approach with complete mobilization of the kidney and its hilum, so that the kidney can be ‘flipped over’ to expose the tumour. During the retroperitoneal approach the angles for suturing are suboptimal for a mid-pole posterior or posteromedial tumour, while these angles are optimal for a posteriorly located apical upper pole or lower pole tumour. As PN requires de-fatting the kidney, having abundant visceral fat around the kidney is relatively detrimental for the retroperitoneal approach, as the loose fat in the retroperitoneum diminishes the working space. Because of the limited space in the retroperitoneum, larger tumours might preferentially be tackled transperitoneally. In a case of multiple renal arteries, en bloc Satinsky clamping or occasionally individual bulldog clamping will suffice.
The technique of LPN is based on contemporary time-tested techniques of OPN . The main technical issues during LPN are: adequate laparoscopic exposure, aligning favourable angles for tumour excision and sutured repair, achieving haemostasis, repair of the collecting system, and reconstructing the parenchymal defect, all within a finite ischaemia time.
EXPOSURE AND PLANNING
This is a subtle and oft-ignored aspect in many descriptions of the technique of LPN. Port-placement and exposure of the kidney and the tumour, so that the margins of excision are in direct line of sight of the camera port, is critically important. While de-fatting the kidney, appropriately located ‘handles’ of perirenal fat and fascia should be left on the kidney surface to allow manipulation during excision and reconstruction. All peritumoral fat must be maintained en bloc over the tumour for oncological reasons; this fat allows elevation of the tumour from the PN bed during excision, so that the resection can be done under excellent vision. Tumour resection should be pre-planned, keeping in mind the suturing angles needed to reconstruct the ensuing defect. The resection itself should be done so that the final defect is shaped like a ‘shallow boat’ rather than a ‘deep well’.
BLOODLESS FIELD AND HAEMOSTASIS
Currently, the only established method of obtaining a near-bloodless field during LPN is to clamp the hilum. We prefer to clamp both the artery and the vein, although some authors only clamp the artery. Suture ligation of divided blood vessels and a sutured parenchymal repair over haemostatic material are used during OPN, and we replicate these in our LPN technique.
Previous RF coagulation has been used as a haemostatic tool during LPN. Potential disadvantages of RF coagulation during LPN are the possibility of collateral damage to the renal vasculature and collecting system, and difficulty in distinguishing coagulated tumour from coagulated normal parenchyma during subsequent excision and histopathological assessment.
WARM ISCHAEMIA (WI)
LPN requires a somewhat longer WI time than OPN ; attempts are made to keep the WI time to <30 min [25,32]. Recent evidence suggests that longer periods of WI might be commensurate with recovery of remnant function . No significant decrease in GFR or increase in serum creatinine level was found even after 90 min of WI in a solitary kidney porcine model, 15 days after the procedure .
The first reported technique of renal hypothermia during LPN involved surface-contact cooling with ice-slush. After mobilizing the kidney and placing an Endocatch-II bag (US Surgical, Norwalk, CT) around it, the hilum was clamped, the bottom of the bag was retrieved through a port site, and ice-slush delivered into the bag to rapidly cool the kidney to 5–19 °C . Another technique to surface-cool the kidneys to 15–25 °C during LPN, in a porcine model using fine ice-slush delivered through a 10-mm laparoscopic end-effector, was recently reported . Janetschek et al. reported continuous perfusion of a crystalloid solution at 4 °C through a percutaneously placed angiocatheter in the occluded renal artery; however, the parenchymal temperature achieved was ≈ 25 °C.
COLLECTING SYSTEM REPAIR
We routinely use a ureteric catheter for the retrograde injection of dilute methylene blue, as it allows us to precisely identify the site of pelvicalyceal entry. Further, after suture-repair, it also allows testing of the water-tightness of the pelvicalyceal repair.
Our current technique of LPN was described earlier . A retrograde 5 F ureteric catheter is placed in the renal pelvis. The patient is positioned 45–60° lateral decubitus for the transperitoneal approach, and 90° lateral decubitus for the retroperitoneal approach. For the retroperitoneal procedure, we prefer to circumferentially mobilize the artery and vein separately, as we prefer individual laparoscopic bulldog clamps (two for the artery and one for the vein) for the retroperitoneal procedure. Transperitoneally, the vessels are not individually mobilized; instead, space is created around the hilum for en bloc Satinsky clamping. The kidney is de-fatted, maintaining fat over the tumour (Fig. 1) and retaining fat-handles at strategic locations on the kidney to allow easy manipulation during LPN. Laparoscopic ultrasonography is used to map the tumour limits with a margin of normal parenchyma; a 5–10 mm margin is considered adequate. Intravenous mannitol is administered 10–20 min before clamping (Fig. 2). The tumour and overlying fat are excised with cold scissors (Fig. 3). The collecting system is suture-repaired with a continuous 2/0 polyglactin suture on a CT-1 needle (Fig. 4). Renorrhaphy (Fig. 5) is performed with three to six interrupted sutures of 1/0 polyglactin on a CT-X needle over a pre-prepared Surgicel bolster (Johnson & Johnson, New Brunswick, NJ, USA). A Hem-o-Lok clip (Weck Closure System, Research Triangle Park, NC, USA) is secured on the suture to prevent it from pulling through. The biological haemostatic agent FloSeal (Baxter Healthcare, Deerfield, IL, USA) is applied to the PN bed underneath the bolster. Another Hem-o-Lok clip is applied to the tightened suture flush against the opposite kidney surface, compressing the parenchyma. The suture is then tied across the defect, on top of the bolster, augmenting compression. Mannitol and frusemide are administered i.v. just before unclamping. The abdomen is re-inspected after 5 min of zero pneumoperitoneum pressure to ensure haemostasis. The specimen is removed in an Endocatch bag and a Jackson-Pratt drain is placed before exiting the abdomen.
PERI-OPERATIVE, FUNCTIONAL AND ONCOLOGICAL OUTCOMES
CLEVELAND CLINIC EXPERIENCE
At a mean (range) follow-up of 42 (24–62) months in 100 patients, the cancer-specific survival was 100%, with no local or distant recurrence, although positive margins were noted in two patients . Five-year data are now available in 50 patients treated at our institution, with a mean (range) tumour size of 3 (1.4–7) cm. The 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 years, the overall and cancer-specific survival was 84% and 100%, respectively .
In the first 200 LPNs at our institution, haemorrhagic complications  occurred in 19 patients (9.5%). Open conversion was required in two (1%) and re-exploration laparotomy in four patients (2%). A urine leak occurred in nine patients (4.5%). With increasing experience and refinement of techniques, our complication rates have decreased significantly (haemorrhage 3% and urine leak 1.5%) .
MULTICENTRE COMPARISON OF LPN WITH OPN
We have recently completed a retrospective comparison, including 1800 patients of LPN (771) with OPN (1029) for a single renal tumour, from three tertiary referral institutions (Cleveland Clinic, Johns Hopkins, and Mayo Clinic) . OPN patients comprised a higher risk surgical group with older patients, larger tumours and more solitary kidneys (P < 0.001 for all). LPN was associated with less operative blood loss, shorter operative time, and shorter hospital stay (P < 0.001 for all). The WI time was ≈ 10 min longer during LPN (P < 0.001). Despite the slightly longer WI time, renal functional outcomes were similar between the LPN and OPN groups, with 97.9% and 99.6% of renal units retaining function. Complications during surgery were similar, while complications afterward were more common for LPN (18.6% vs 13.7%). Specifically, haemorrhage occurred in 4.2% after LPN and 1.6% after OPN. Positive surgical margins for RCC were similar, at 1.6% vs 1%; oncological outcomes were also similar, with local recurrence in 1.4% vs 1.5%, and distant recurrence in 0.9% vs 2.1%, after LPN and OPN, respectively. The 3-year estimated cancer-specific survival was 99.3% and 99.2% in the two groups, respectively. Peri-operative [43–47] and oncological outcomes [38,39,43,45,46,48] from selected LPN studies are listed in Tables 2 and 3, respectively.
Table 2. Perioperative outcomes after LPN
Number of patients
WI time, min
Tumour size, cm
These 200 consecutive patients comprise a contemporary cohort from our overall experience of 625 patients undergoing LPN. NA, NA, not available.
As laparoscopic techniques and technology advance, LPN will be used increasingly worldwide. Safe methods of unclamped LPN and bloodless techniques for parenchymal incision need to be defined. The feasibility of the 80 W potassium-titanyl-phosphate laser  and hydrojet dissection  for unclamped LPN were reported by our team in the survival bovine model. At present, these technologies have yet to be applied in clinical LPN. Current techniques for laparoscopic renal hypothermia are cumbersome and hence avoided by most laparoscopic surgeons. A user-friendly method that reproducibly reduces renal temperature to 15 °C might extend the indications for LPN.
Nearly a third of small renal masses treated by NSS are benign; these patients could potentially avoid an operation if there was a foolproof method to distinguish benign from malignant masses before surgery; at present there is no such method.
Other potential advances could include extracorporeal methods of treating small renal mass; these include high-intensity focused ultrasound and radiosurgery . Most such techniques are still experimental.
NSS is currently the preferred treatment for the small renal mass. OPN, by establishing the fundamental principles of NSS, has been the reference standard. LPN, by duplicating the principles and outcomes of OPN, appears to be the method of the future. LPN is the minimally invasive technique of choice for NSS and is becoming standardized and more prevalent around the world. Preliminary 5-year oncological data for LPN are just becoming available, and in skilled hands the outcomes are similar to OPN. In the near future LPN will probably become the preferred option for most renal tumours of <7 cm, while OPN will be reserved for patients with a tumour that requires complicated excision and reconstruction.