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Volume 57, issue 2, pages 179-362, February 2010

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A Critical Analysis of the Actual Role of Minimally Invasive Surgery and Active Surveillance for Kidney Cancer

Roman Heuer a lowast , Inderbir S. Gill b, Giorgio Guazzoni c, Ziya Kirkali d, Michael Marberger e, Jerome P. Richie f, Jean J.M.C.H. de la Rosette g.

Accepted 13 October 2009, Published online 20 October 2009, pages 223 - 232

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Abstract

Context

The incidence of renal cell carcinomas (RCCs) has increased steadily—most rapidly for small renal masses (SRMs). Paralleling the changing face of RCC in the past 2 decades, new, less invasive surgical options have been developed. Laparoscopic radical nephrectomy (LRN) is an established procedure for the treatment of RCC. Treatment of SRMs includes open partial nephrectomy (OPN), laparoscopic partial nephrectomy (LPN), thermal ablation, and active surveillance.

Objective

To present an overview of minimally invasive treatment options and data on surveillance for kidney cancer.

Evidence acquisition

Literature and meeting abstracts were searched using the terms renal cell carcinoma, minimally invasive surgery, laparoscopic surgery, thermal ablation, surveillance, and robotic surgery. The articles with the highest level of evidence were identified with the consensus of all the collaborative authors and reviewed.

Evidence synthesis

Renal insufficiency, as measured by the glomerular filtration rate, occurs more often after radical nephrectomy than partial nephrectomy (PN). OPN and LPN show comparable results in long-term oncologic outcomes. The treatment modality for SRMs should therefore be nephron-sparing surgery (NSS). In select patients, thermal ablation or active surveillance of SRMs is an alternative.

Conclusions

LRN has become the standard of care for most organ-confined tumours not amenable to NSS. Amongst NSS options, PN is the treatment of choice, yet remains underutilised in the community. Initial data during its learning curve revealed that LPN had higher urologic morbidity. However, current emerging data indicate that in experienced hands, LPN has shorter ischaemia times, a lower complication rate, and equivalent long-term oncologic and renal functional outcomes, yet with decreased patient morbidity compared to OPN. Robotic partial nephrectomy is being explored at select centres, and cryotherapy and radiofrequency ablation are options for carefully selected tumours. Active surveillance is an option for selected high-risk patients. Percutaneous needle biopsy is likely to gain increasing relevance in the management of small renal tumours.

Take Home Message

Because preservation of renal function is paramount, partial nephrectomy must be considered the treatment of choice for surgical small renal masses (SRMs). At centres of excellence, laparoscopic partial nephrectomy outcomes now equal open partial nephrectomy outcomes for most patients with an SRM. Newer ablative techniques and active surveillance programs offer alternative treatment options for select high-risk patients.

Keywords: Renal cell carcinoma, Minimally invasive surgery, Laparoscopic surgery, Thermal ablation, Surveillance, Robotic surgery.

Article Outline

1. Introduction

1.1. Epidemiology of kidney cancer: rising incidence, stage migration

The incidence of renal cell carcinoma (RCC) has increased steadily between 1975 and 2002 [1], and [2]. Incidence has increased most rapidly for localised tumours, probably because of improved noninvasive diagnostic imaging [1]. From 1988 to 2002, the average renal tumour size decreased from 67 mm to 59 mm, according to an analysis of data from the Surveillance, Epidemiology, and End Results (SEER) database. Analysis of a large European cohort showed that the general incidence of surgically removed renal cancers increased from 6.2 to 7.5 per 100 000 patients, the incidence of T1 tumours increased from 36.6% to 44.2%, and advanced tumours decreased from 46.4% to 33.7% during the period 1995–2005 [3]. The number of patients presenting with tumours <4 cm increased from 30% to 39%. Improved survival in more recently diagnosed patients could be attributed to these trends [2].

In response to the changing presentation of RCC in the past 2 decades, new surgical options have been developed. Laparoscopic radical nephrectomy (LRN) is now one of the standard treatment options. Based on the experience of open nephron-sparing surgery (NSS) procedures, laparoscopic partial nephrectomy (LPN) was introduced, and ablative strategies for selected patients further represent minimally invasive treatment alternatives.

return to article outline

2. Evidence acquisition

Literature and meeting abstracts were searched using the terms renal cell carcinoma, minimal invasive surgery, laparoscopic surgery, thermal ablation, surveillance, and robotic surgery. The articles with the highest level of evidence for the various examined end points were identified with the consensus of all the collaborative authors and were reviewed. More than 65% of the citations were published in 2006 and later, with >90% in the past 10 yr.

return to article outline

3. Evidence synthesis

3.1. Laparoscopic radical nephrectomy

LRN was first introduced by Clayman in 1991 [4]. He described a transperitoneal approach, but LRN can also be performed retroperitoneoscopically and hand-assisted transperitoneally [5]. Desai et al compared the transperitoneal and the retroperitoneal approach: 102 patients were randomised into two groups. The retroperitoneoscopic approach had a shorter time to control of renal hilus and shorter total operative time but did not show differences in the other patient outcomes evaluated [6]. In another retrospective study with 100 patients, no differences in the two approaches were found [7]. LRN has benefits over open radical nephrectomy (ORN) in terms of cosmetic outcome, convalescence, duration of hospital stay, and blood loss [8].

From an oncologic point of view, 5-yr follow-up data show comparable results in organ-confined disease (T1 and T2) when comparing LRN with ORN. Overall survival (OS) and cancer-specific survival (CSS) were comparable, with no significant difference [8], and [9]. For T2 tumours, Hemal et al showed that LRN has no difference in 5-yr survival and is effective with less blood loss, shorter hospital stay, decreased analgesic requirement, and rapid recovery compared with ORN [8]. Permpongkosol et al presented a 10-yr follow-up of T1 and T2 tumours treated with either transperitoneal LRN or ORN. Disease-free survival (DFS) rates, CSS, and OS did not reveal any significant difference [10].

LRN has also been applied to locally advanced tumours. In a three-arm study, Gill's group compared ORN patients (n = 39) and LRN patients (n = 65) for tumours >7 cm with LRN patients (n = 166) for tumours <7 cm. Blood loss was less and operation time was shorter in both LRN groups compared to the ORN arm. LRN for tumours >7 cm in size appears to be equivalent in terms of positive surgical margins (PSMs) compared to ORN [11]. Portis et al reported 5-yr follow-up data showing 97% CSS and 92% recurrence-free survival for tumours >7 cm after LRN [12]. Simmons et al showed that laparoscopic lymph node dissection and nephrectomy for advanced or metastatic RCC is possible and safe in select patients and specialised centres and, because of its decreased morbidity, is beneficial in patients with advanced disease [13].

LRN has benefits over ORN, especially in terms of morbidity, and should be the standard of care for T1 and T2 tumours when available and nephron-sparing treatment is not applicable.

3.2. Partial nephrectomy

For small, localised tumours, NSS is the reference standard, as partial nephrectomy (PN) leads to reduced impairment of renal function compared to radical nephrectomy (RN). Even when preoperative risk factors for renal insufficiency are controlled for, patients undergoing ORN are at a greater risk of chronic renal insufficiency than a similar cohort of patients undergoing PN, with the oncologic outcome being equivalent in both groups [14]. The 3-yr probability of absence of new-onset of glomerular filtration rates (GFRs) <60 ml/min per 1.73 m2 in a retrospective study of 662 patients who underwent elective partial or radical nephrectomy for a solitary tumour was 80% (95% confidence interval [CI], 73–85) after PN and 35% (95% CI, 28–43; p < 0.0001) after RN [15].

Furthermore, the risk of death, cardiovascular events, and hospitalisation has an independent, graded association with a reduced estimated GFR [16]. Compared to ORN, PN has comparable costs [17], and overtreatment by nephrectomy for benign tumours is avoided [18]. Oncologic results are similar to those found after RN, with better preservation of renal function [19], and [20]. In select patients, even localised RCC larger than T1a can be treated with elective NSS, providing good long-term outcomes [20].

Two scoring systems using algorithms to standardise and quantify the anatomical features and allow prediction of risk of complications of small renal masses (SRMs) undergoing excision are available. These tools can be used to stratify patients into complication subgroups and improve comparability [21], and [22].

3.3. Laparoscopic partial nephrectomy
3.3.1. Early experience

Advances in laparoscopic skills made it possible to transfer the techniques of OPN to LPN to treat SRMs laparoscopically. In select centres, LPN today is an established alternative treatment for T1a tumours [23]. LPN can be performed retroperitoneoscopically or, preferentially, transperitoneally. The choice of approach is based on the tumour location and size as well as the experience of the surgeon [9], and [24]. LPN has the advantages of reduced operative time, decreased operative blood loss, and a shorter hospital stay compared to OPN [25], but LPN is technically demanding, and longer ischaemic time and haemostasis concerns remain.

In a recent multicentre study, Gill et al compared the most recent 1039 patients undergoing OPN with the very initial 771 patients undergoing LPN for a single renal tumour <7 cm [25] (Table 1). Postoperative renal function was similar (97.9% vs 99.6% functioning renal units after 3 mo), but urologic complications were more common in the LPN group (odds ratio [OR]: 2.14; 95% CI, 1.39–3.31). For postoperative haemorrhage, the OR was 3.51 (95% CI, 1.82—6.77), favouring the OPN group. However, equivalent functional and early oncologic outcomes were achieved. It is of interest that risk distribution in the two groups was not identical. The Eastern Cooperative Oncology Group (ECOG) performance status was better in the LPN group, median tumour size was smaller, renal function was less impaired, and fewer patients presented with symptomatic disease. Based on these data, the preoperative risk distribution in the LPN group was favourable. In their retrospective analysis, Simmons et al evaluated the use of LPN for tumours >4 cm in size (n = 58) [26]. There were no increased risks for positive margins or intraoperative or postoperative genitourinary complications for tumours >4 cm when compared with two groups—one with tumour size <2 cm (n = 89) and the other with tumour size 2–4 cm (n = 278).

Table 1 Retrospective analysis of open partial nephrectomy (OPN) versus laparoscopic partial nephrectomy (LPN) in 1800 patients [25]

LPN OPN p value
Patients, No. 771 1029 –
Mean blood loss 300 376 <0.0001
Operating time, min 201 266 <0.0001
Warm ischaemia time, min 30.7 20.1 <0.0001
Mean tumour size, cm 2.6 3.3 <0.0001
ECOG status ≥1, % 1.4 14.7 –
Duration of hospitalisation, d 3.3 5.8 <0.0001
Postoperative complications 18.6 13.7 <0.0001
Subsequent procedures, % 6.9 3.5 <0.0001
3-yr survival, % 99.3 99.2 NS

ECOG = Eastern Cooperative Oncology Group; NS = not significant.

In another recently published retrospective analysis by Simmons et al, intermediate-term oncologic and functional outcome after LPN (n = 35) was compared with LRN (n = 75) [27]. Median follow-up was 57 mo for LRN and 44 mo for the LPN group. Overall mortality was 11% versus 11%, and CSS was 3% versus 3%. No statistically significant difference in incidence of local recurrence was found in the LPN group (6% vs 3%). After LRN, 12% of patients had a two-stage increase in chronic kidney disease versus 0% in the LPN group.

A comparison of LPN and OPN for tumours <7 cm in size in a solitary kidney was performed recently. Results of the 169 open and 30 laparoscopic PNs were retrospectively investigated. Decrease of the GFR was 21% in the OPN group and 28% in the LPN group (p = 0.24). Postoperative need of dialysis occurred in one (0.6%) of the OPN patients and in three (10%) of the LPN patients (p = 0.01). End-stage renal failure after 1 yr of follow-up was found in 0.6% of the OPN patients and 6.6% of the LPN patients (p = 0.06). Warm ischaemia time was 9 min longer in the LPN group (p = 0.0001). For patients at risk for chronic kidney disease, OPN may be the treatment of choice [25], and [28]. However, data for the subgroup of T1a tumours <4 cm were not specifically evaluated.

When compared with OPN, the rate of PSM after LPN was similar. Table 2 shows the six largest series published to date. Also, from the long-term oncologic point of view, LPN seems to be comparable to OPN, with similar results (Table 3).

Table 2 Positive surgical margin (PSM) rate: laparoscopic partial nephrectomy (LPN) versus open partial nephrectomy

Patients, No. PSM, % Tumour size, mean
LPN Breda et al [73] 808 2.4 2.7
Gill et al [25] 556 1.6 2.6
Permpongkosol et al [74] 511 1.8 2.8
OPN Gill et al [25] 858 1 3.3
Kwon et al [75] 770 7.4 2.6
Patard et al [76] 542 1.5 3.4

Table 3 Oncologic long-term results of laparoscopic partial nephrectomy (LPN) and open partial nephrectomy (OPN)

Approach Patients, No. pT1 stage, % FU/year DFS after 5 yr, % CSS after 5 yr, % CSS after 10 yr, %
Lane et al [23] LPN 37 92 5 97 100 –
Permpongkosol et al [33] OPN 58 100 5 97.6 – –
Permpongkosol et al [33] LPN 85 100 5 91.4 – –
Fergany et al [19] OPN 107 60 5/10 – 97.6 94.5

FU = follow-up; DFS = disease-free survival; CSS = cancer-specific survival.

3.3.2. Contemporary data

As noted above, the initial LPN data indicated somewhat longer ischaemia times compared to OPN. However, the increasing experience with LPN and the development of an “early unclamping” technique has significantly decreased ischaemia times, allowing superior LPN outcomes. Specifically, LPN ischaemia times have now been decreased by >50%, to a mean of 14 min currently [29], [30], and [31].

Gill et al recently reported a single-surgeon series of 800 LPN cases encompassing a 9-yr period (1999–2008) [32]. The authors divided the entire cohort into three chronologic eras: Era I (1999–2003; n = 276), Era II (2004–2006; n = 289), and Era III (2007–2008; n = 235). In comparing Eras I, II, and III, tumours in the most recent era were larger (more commonly >4 cm) and central, with peripheral masses <4 cm less common (p < 0.05 for all). Despite this increasing tumour complexity, mean warm ischaemia times were shorter in the most recent era: 32 min, 32 min, and 14 min, respectively (p < 0.0001). Overall, postoperative, and urologic complications were significantly lower in the most recent era. Finally, renal functional outcomes were superior in Era III, as documented by a lesser percent decrease in estimated GFR (18%, 20%, and 11%, respectively).

Kamoi and Gill (unpublished data) also retrospectively compared 150 contemporary patients undergoing OPN between 2006 and 2008 with 150 contemporary patients undergoing LPN between 2007 and 2008. Notably, all OPNs were performed by one experienced open surgeon (A.C. Novick), and all LPNs were performed by one experienced laparoscopic surgeon (I.S. Gill). After controlling for differences in baseline demographics, LPN patients had shorter ischaemia times (21 vs 13 min, p < 0.0001), more LPN patients had ischaemia times <20 min (52% vs 97%), and fewer had ischaemia time >30 min (9% vs 0%; p < 0.001 for both). Postoperative complications were fewer in the LPN group (19% vs 8.7%; p = 0.01), including haemorrhage (3.3% vs 2.7%; p = ns) and urine leak (7.3% vs 1.3%; p = 0.02). Patients undergoing elective PN had similar renal functional outcomes, and those undergoing imperative PN or PN in a solitary kidney had superior renal functional outcomes in the LPN cohort, probably as a result of the reduced ischaemic insult during LPN.

These contemporary data suggest that, despite increasing tumour complexity, three key outcomes of contemporary LPN (ischaemia time, complications, and renal function) have improved significantly. In experienced hands, LPN now rivals OPN, albeit with vastly decreased patient morbidity. LPN delivers 5-yr and 7-yr oncologic results similar to OPN [33].

Consequently, expert laparoscopic surgeons offer LPN for tumours until now reserved for OPN: larger (cT1b) tumours, central tumours, completely intraparenchymal tumours, multiple tumours, hilar tumours, and tumours in a solitary kidney (unpublished data). In the near future, we anticipate that at tertiary centres of expertise, LPN will likely replace OPN as the reference standard treatment for the majority of patients with a surgical SRM.

3.4. Robotic partial nephrectomy

Well established for the treatment of prostate cancer (PCa), robotic surgery is now being used in the treatment of RCC. Oncologic data presented so far are immature because of a lack of follow-up. In the largest series published, Rogers et al retrospectively analyse the outcome of 148 patients undergoing robotic partial nephrectomy (RPN) for renal neoplasm (mean tumour size: 2.8 cm; range: 0.8–7.5 cm) [34]. PSM was seen in six (4%) patients. Mean warm ischaemia time was 28 min, mean operating time was 197 min, and postoperative complications were found in 9 (6.1%) patients. In another series, Wang et al analysed data from 102 patients. Forty patients underwent RPN, and 62 underwent LPN. There was no significant difference in tumour size (2.5 vs 2.4 cm), blood loss, or incidence of PSM (one vs one patient). Total operative time (140 vs 156 min) and warm ischaemia time (19 vs 25 min) were significantly shorter for the RPN group [35]. A matched-pair analysis of RPN against LPN (12 patients in each group) showed no differences in perioperative parameters (warm ischaemic time, blood loss, operating time) [36].

In a recent retrospective analysis of 118 LPN versus 129 RPN patients from three academic centres, the outcome in terms of warm ischaemic time, intraoperative blood loss, and length of hospital stay were significantly better in the RPN group [37]. PSM, overall operating time, and pathologic tumour size were equivalent in both groups.

From the preliminary data available, it can be derived that RPN is technically feasible and safe. To determine the value of RPN for treatment of RCC, however, further studies and longer follow-ups are necessary.

3.5. Ablative treatment modalities/active surveillance
3.5.1. High-intensity focused ultrasound

An extracorporeal approach for ablation of renal masses by high-intensity focused ultrasound (HIFU) has faced major technical difficulties. In a phase 2 study, the effect of HIFU on SRM was evaluated. Results showed shrinkage of tumours in 9 of 14 kidneys, but in histopathologic examination, only 15–35% of the actual tumour volume showed necrosis [38]. In another series of 19 patients who underwent extracorporeal HIFU, 15 showed limited morphologic signs of thermal injury, but lesion size was never reached [39].

In a recent phase 1 study, laparoscopic intracorporeal HIFU ablation of small renal tumours has been investigated. Of the 10 patients, 3 showed viable tumour cells after treatment [40]. Currently, HIFU does not seem to be a valuable option for treatment of SRM but might become an option in the future if the technical difficulties are overcome.

3.5.2. Cryoablation

As an alternative treatment for localised renal masses <4 cm in size, other minimally invasive nephron-sparing modalities than LPN, such as radiofrequency ablation (RFA) or cryoablation, have emerged. For patients who may not be suitable for conventional or laparoscopic surgical excision, these thermal ablations could be a less invasive method of treatment. Both ablative modalities can be performed open, laparoscopically, or percutaneously. Benefits of these treatments are the minimal invasiveness and short hospitalisation times. A disadvantage in contrast to the surgical excision is that the tumour remains in the kidney, and oncologic radicality cannot be evaluated. At the moment, follow-up is limited, and the success criteria for complete tumour depletion are inconclusive.

When cryoablation of the kidney was introduced in 1995 [41], open surgery was initially used [42]. With more experience, a laparoscopic approach for anterior and percutaneous or retroperitoneoscopic approaches for posterior tumours was used. Ultrasound can be used to place the probes, and ice ball formation can be monitored during ablation. Under cryoablation, real-time monitoring of mass destruction by visualising the ice ball formation is possible. Cryoablation causes cell destruction during the freeze and thaw temperature cycles. A temperature <19.4 °C leads to complete cell death [43]. If ice ball formation extends beyond the tumour by >3.1 mm, a temperature <20 °C is reached in the tumour tissue [44]. Table 4 shows the results of selected published series of laparoscopic, open, and percutaneous cryotherapy.

Table 4 Selected series of cryoablation

Approach Tumours, No. Median size, cm Follow-up, mo CSS, % Tumour recurrence after one ablation, %
Gill et al [77] Laparoscopic 56 (36 proven RCCs) 2.3 36 98 3.6
Schwarz et al [78] Open/laparoscopic 85 (50 proven RCCs) 2.6 10 (mean) – 2.4
Davol et al [79] Open/laparoscopic 48 (38 proven RCCs) 2.6 64 (median) 100 12.5, 2.5*
Hegarty et al [57] Laparoscopic 179 (no. of RCC not given) 2.5 36 (median) 98 1.7
Cestari et al [80] Laparoscopic 37 (29 proven RCCs) Mean: 2.6 20.5 (mean) – 5.7
Silvermann et al [81] Percutaneous 26 (24 proven RCCs) 2.6 14 (mean) – 13
Aron et al [82] Laparoscopic 88 (no. of RCC not given) 2.3 83 (median) (range: 60–120) At 5 yr: 95 At 5 yr: 22

CSS = cancer-specific survival; RCC = renal cell carcinoma.

* After first and after repeat treatment cycle.

Finley et al compared 24 tumours undergoing laparoscopic cryoablation and 19 tumours treated with percutaneous cryoablation [45]. The overall complication rate was lower in the percutaneous group (22.2% vs 40%), and the hospital stay was shorter (1.3 vs 3.1 d; p < 0.0001). CSS after 11.4 mo for the percutaneous group and after 13.4 mo for the laparoscopic group was 100%. The treatment failure rate was 5.3% and 4.2%, respectively.

Laguna et al evaluated the perioperative morbidity of laparoscopic cryoablation in a European multicentre study [46]. They described 148 procedures in 144 patients with a median age of 70.5 yr and median tumour size of 2.6 cm (range: 1.0–5.6). Perioperative negative outcomes, including conversion, were seen in 17% of cases treated. Complications according to the Clavien system occurred in 15.5% of cases; most of the complications were Clavien grade 1 and 2, and grade 3 complications occurred in 4% of cases. Only one-third of the complications were the result of the cryoablation procedure. The presence of cardiac conditions, female gender, and tumour size were independent prognostic factors for the occurrence of a perioperative negative outcome.

Criteria for successful ablation are still not finalised, but shrinkage of the lesion and lack of contrast uptake in subsequent imaging are surrogate parameters for successful ablation. Increasing volume and contrast uptake are used to define failure of treatment. Beemster et al [47] followed 26 patients with laparoscopic cryoablation for ≥6 mo and found nonenhancing infiltration of the perirenal fatty tissue in all, a decrease of diameter of the lesion in mean by 38% in 12 mo, and rim enhancement in 20% of cases. All of these findings were independent of the histopathologic diagnosis.

Postoperative evaluation of cryoablation results with magnetic resonance imaging (MRI) in 18 patients with follow-up between 6 and 48 mo were presented by Bolte et al [48]. Peripheral rim enhancement was a common finding on MRI. Rim enhancement with an increase in lesion size or nodular enhancement was found to be more suspicious than rim enhancement alone.

3.5.3. Radiofrequency ablation

RFA converts radiofrequency waves to heat, delivering temperatures >50 °C to tissue and resulting in coagulation and necrosis. Optimal tissue ablation is achieved when the temperature is >50 °C but <100 °C. Temperatures >100 °C result in tissue vaporisation, leading to insufficient conductivity and transmission of energy to the tissue [49]. RFA can be applied in monopolar and bipolar configurations, with less risk of skin burns in the bipolar technique [50]. In the literature, RFA is mostly applied percutaneously to small renal lesion but can also be used in an open or laparoscopic surgery setting. Table 5 shows the results of selected series of RFA.

Table 5 Selected series of radiofrequency ablation

Approach Tumours, No. Median tumour size Follow-up, mo CSS, % Tumour recurrence after one ablation, %
Zagoria et al [51] Percutaneous 125 (125 RCCs) 2.7 13.8 (mean) 98 13*
McDougal et al [52] Percutaneous 20 (all RCCs) 3.2 55.2 (median) 94 5
Hegarty et al [57] Percutaneous 82 (no. of RCC not given) 2.5 12 (median) 100 11.1
Park et al [83] Laparoscopic/percutaneous 94 (65 RCCs) Mean: 2.4 25 (mean) 98.5 3.2

CSS = cancer-specific survival; RCC = renal cell carcinoma.

* All tumours recurring were >3.7 cm.

Zagoria et al evaluated computed tomography (CT)–guided percutaneous RFA of 125 biopsy-proven RCCs in a single-institution series [51]. The tumour size ranged from 0.6 to 8.8 cm (mean: 2.7; standard deviation: 1.5 cm). All 95 RCCs smaller than 3.7 cm were completely ablated, but nine of the larger tumours showed evidence of residual tumour. A tumour size <3.7 cm was significantly associated with complete tumour eradication (p < 0.001). The longest follow-up is available from the analysis of McDougal et al [52] but is limited because of the small number of patients. Data were reported from 16 patients (20 tumours) who underwent RFA, with a minimum follow-up of 4 yr. Of the 16 patients, 5 died of unrelated causes, and 1 had recurrent disease.

In RFA, as in cryoablation, no radiologic criteria for successful ablation are available. Klingler et al [53] found a tumour recurrence rate of 18% (4 of 22) in a series of patients who underwent RFA with state-of-the-art technology prior to LPN. This study confirms the results of other working groups [54], and [55].

3.5.4. Radiofrequency ablation versus cryoablation

Weight et al retrospectively analysed data from 109 renal lesions in 88 patients who were ablated with percutaneous RFA and 192 lesions in 176 patients who underwent laparoscopic cryoablation [56]. Patients were followed up with radiographic imaging and postablation biopsy at 6 mo. The authors found that radiographic follow-up was negative in 85% (62 cases) and 90% (125 cases) for RFA and cryoablation, respectively. A total of 134 lesions (45%) were then biopsied; viable tumour cells were found in 25% of patients in the RFA group. In the cryoablation cohort, no remaining tumour was found in 93.8% of patients. Six of the 13 patients with positive biopsy after RFA demonstrated no enhancement on post-treatment imaging. In the cryoablation group, all patients having positive biopsies had positive enhancement on imaging.

In a retrospective, single-centre analysis, Hegarty et al compared 164 (179 tumours) laparoscopic cryoablations and 82 percutaneous RFAs [57]. Tumour size was equal (2.56 vs 2.51 cm), but in the cryoablation group, central tumours (6% vs 37%) and solitary kidneys (24% vs 49%) were less common. The rate of radiologic relapse of tumour was 1.8% in the cryotherapy group versus 11.1% in the RFA group. CSS was 98% in the cryotherapy group after 3 yr of follow-up and 100% for the RFA group after 1 yr of follow-up. Although selection bias was present, cryotherapy seems to result in more consistent and reliable tumour destruction. Both ablation techniques have a low complication rate, with the majority of incidences being minor complications that require observation only [58].

In their meta-analysis of cryoablation versus RFA, Kunkle and Uzzo evaluated treatment outcome of 1375 lesions in the kidney [59]. Six hundred patients were treated by cryoablation (65% laparoscopically) and 775 by RFA (94% percutaneously). Local tumour progression was more frequent after RFA (12.9% vs 5.2%). Pretreatment biopsy was performed more frequently in the cryoablation group (82.3% vs 62.2%). The rate of repeat ablation was higher in the RFA group (8.5% vs 1.3%). Metastases were reported less commonly in the cryoablation group (1.0% vs 2.5%; p = 0.06).

Cryoablation has a lower reablation and local recurrence rate and good intermediate oncologic outcomes [57], and [59]. In terms of metastatic progression, no statistical differences were found [59]. Data for the ablation techniques are still not mature, but early results seem promising. Especially for RFA, the problem of viable tumour cells after ablation remains unsolved. For both kinds of thermal ablation, long-term radiographic monitoring is mandatory, and renal biopsy should be included in follow-up protocols to improve measurement of oncologic efficacy. Further prospective studies and longer follow-up are necessary to determine long-term oncologic efficacy for both RFA and cryoablation. However, for select patients with SRMs <4 cm and who are at a high surgical risk, ablative techniques are a therapeutic alternative.

3.5.5. Active surveillance

Although the standard of care for SRMs is surgical excision, the question of whether treatment is beneficial and necessary for all patients arises. Can surveillance be recommended to a patient with an incidental renal mass with medical comorbidities and a limited life expectancy, similar to patients with diagnosis of PCa? Many T1 renal masses are benign (20%) and can be managed less aggressively; nevertheless, 20–30% of the tumours show aggressive features. A 17% rise in the incidence of malignancy for every 1 cm more in size of tumour was found [60], and [61].

For small renal lesions, median growth rate and, most important, risk of metastasis have been investigated. In their meta-analysis, Chawla et al evaluated 234 small renal lesions. Median size was 2.48 cm (range: 1.73–4.08), and the mean growth rate at a mean follow-up of 34 mo was 0.28 cm per year. A total of 131 tumours were biopsied. In biopsy-confirmed RCC (n = 120), the mean yearly growth rate was 0.4 cm. Progression to metastatic disease was identified in 1% of lesions, and a subset of 30% of tumours showed no growth [62]. Remzi et al analysed 287 small renal lesions that were removed surgically [60]. One hundred sixty-eight patients had tumours <3 cm; of these, four patients (2.3%) had metastatic disease. Of the 119 patients with tumour size >3 cm, metastases were found in 10 (8.4%). The authors conclude that the aggressive potential increases beyond a diameter of 3 cm. These data are further supported by another retrospective series by Crispen et al [63]. One hundred nine patients with 124 small renal lesions (median age: 73 yr; median tumour size: 2.0 cm) were evaluated. The median duration of active surveillance was 26 mo. Of the 64% of patients under surveillance, one (1.4%) developed metastatic disease.

In terms of CSS, Abouassaly et al retrospectively reviewed data from 110 patients with a median age of 81 yr [64]. The median follow-up was 24 mo. The mean tumour growth rate was 0.26 cm per year. Thirty-four patients had died at the conclusion of the study for reasons other than the renal mass, and CSS was 100%. Similar results were found in a retrospective analysis from Beisland et al [65], who evaluated 63 patients with renal masses undergoing observation. Mean tumour size was 4.3 cm, and the mean age of patients was 76.6 yr. Five-year CSS was 93.3%, and 5-yr OS was 42.8%. For tumours <5 cm in size, the 5-yr CSS was 100%. A limitation of this study was that only 28% of the patients had a biopsy of the tumour, with 17% of those having benign histology. Crispen et al came to similar results when retrospectively analysing data from 82 patients (87 SRMs) who received delayed treatment [66]. The median age was 66 yr. The median time from diagnosis to treatment was 14 mo (mean: 21 mo), and the mean tumour size was 2.0 cm. Sixty-two tumours were removed surgically, 25 were ablated, and all tumours underwent biopsy prior to ablation therapy. RCC was found in 84% of tumours. The median growth rate of tumours was 0.19 cm per year. No new onset of metastatic disease was found under observation or after surgery, and the option of minimally invasive NSS was not affected by the delay in treatment. The estimated 1-yr CSS rate was 100%, 99% for 3 yr.

Jewett et al followed 151 renal masses in 131 patients undergoing active surveillance in an ongoing multicentre prospective phase 2 trial [67]. Serial imaging was performed at baseline, 3 mo, and 6 mo, then every 6 mo thereafter. The mean tumour diameter at diagnosis was 2.2 cm (median: 2.1; range: 0.4–4 cm). Of the 72 biopsies performed, 61% showed malignancy, 13% were benign, and 26% were nondiagnostic. Mean follow-up was 15 mo. The average growth rate did not differ from zero (0.35 mm/yr; p = 0.08). Two patients developed metastatic RCC, and seven patients met criteria for tumour progression. Seven patients died from unrelated causes, and 18 patients were withdrawn because of patient or surgeon preference, of which 11 were treated and 7 were lost to follow-up.

In conclusion, imaging alone is insufficient to distinguish between benign and malignant lesions and cannot give information about the aggressiveness of the tumour or the feasibility of active surveillance. No conclusion about the dignity of the lesion can be drawn from the growth rate [68]. Nevertheless, in selected patients, delaying or avoiding treatment seems to be an alternative to surgical or ablative strategies.

The aggressive potential of a renal mass cannot be exactly predicted, even with the use of renal core biopsy, but for patients with SRMs <3 cm who are unfit for intervention or have limited life expectancy, active surveillance offers a treatment alternative with a small risk of cancer progression.

3.6. Renal biopsy

The impact of renal biopsy on treatment of small renal lesions is still controversial. Renal biopsy is only useful if the result will change the course of treatment. Because small, incidentally discovered renal lesions may be benign in a substantial percentage of patients, biopsy to confirm malignancy is important either prior to or at the time of utilisation of minimally invasive ablation techniques. The results of selected recent studies investigating the value of renal core biopsy are shown in Table 6.

Table 6 Results of selected renal biopsy series

Lesions, No. Surgically removed lesions after biopsy, No. (%) Mean tumour size, cm Sensitivity, % Accuracy of biopsy compared with surgical specimen, % Accuracy grading, % Accuracy subtype, % Inconclusive, %
Schmidbauer et al [84] 78 78 (100) 4 94 96 76 91 3
Neuzillet et al [85] 88 62 (70) Median: 2.8 – 92 69.8 92 9.1
Volpe et al [69] 100 20 (20) Median: 2.4 – 100 – 100 16
Lebret [86] 119 64 (53) 3.3 – 86 46 86 21
Shannon et al [87] 235 108 (46) Median: 2.9 – 100 – 98 22
Kümmerlin et al [88] 62 62 (100) 5.5 – 77–90 64–81 64–81 8–16

In summary, the literature shows that biopsy of renal masses can provide an accurate differentiation between malignant and benign tissue in >90% of cases. The rate of inconclusive biopsies ranges from 3% to around 20%. Significant bleeding is unusual, and most biopsies are performed under CT guidance. Limitations of biopsy are hybrid tumours and cystic tumours where malignant tissue is hit by chance. Larger tumour size (<4 cm) and a solid pattern are significant predictors of a diagnostic result for biopsies of renal tumours [69]. Tumour seeding after renal biopsy has a low incidence, and to our knowledge, only six cases are published, all of them prior to 1993. The overall estimated risk is <0.01% [70]. In confirming the success of ablative treatment, renal biopsy can add information to radiographic imaging [56]. Accuracy and standardisation of criteria for renal biopsy has to be further investigated, especially for nondiagnostic biopsies and the diagnosis of benign tumours.

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4. Conclusions

For most large renal tumours that cannot be removed by NSS, LRN is the method of choice. Even for tumours greater than T2, LRN can be safely applied, and the long-term oncologic outcome is comparable to ORN. Because of the existence of promising alternative treatments, indications for ORN are being reduced.

LPN, ablation, and surveillance are minimally invasive or noninvasive treatment options for SRMs. Long-term data are available for NSS and have demonstrated good outcomes. For the ablative therapies, short-term and intermediate-term oncologic outcomes are available. Proof of extended oncologic efficacy is lacking for ablation and surveillance strategies. Initial active surveillance with delayed treatment for progression in selected patients with SRMs can be considered [71], with renal biopsy being helpful in differentiating malignant from benign small renal lesions with the limitations given above. Use of renal biopsy for better diagnosis and classification of SRMs should be considered before deciding on an ablative therapy or surveillance strategy. So far, no criteria are set up for identification of patients who would be potential candidates for active surveillance. Further prognostic factors from either renal biopsy or radiographic imaging are needed. Surgery is still the reference standard and should be performed when possible. Active surveillance should not be recommended to young or healthy patients, but for a highly select subset of patients, it can be recommended as a possible alternative.

Among the ablative therapies, cryoablation seems to have better local tumour control with lower reablation and local recurrence rates and less viable tumour cells in post-treatment biopsies. Both modalities offer treatment alternatives to patients who are not candidates or who decline surgery.

For PN, new techniques are becoming available. RPN becomes more interesting, and data published so far show equal intermediate oncologic outcomes when compared with the other modalities. Warm ischaemic time is shorter compared to LPN. Nevertheless, data presented so far are still immature, and longer follow-up and larger randomised series are awaited.

Unfortunately, most T1a lesions in the kidney are still treated by RN, and NSS is underused [72]. It should be important for the future to ensure that NSS, independent of the technique, is used in every eligible patient with SRM.

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Author contributions: Roman Heuer had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Heuer, Gill, Guazzoni, Kirkali, Marberger, Richie, de la Rosette.

Acquisition of data: Heuer, Gill, Guazzoni, Kirkali, Marberger, Richie, de la Rosette.

Analysis and interpretation of data: Heuer, Gill, Guazzoni, Kirkali, Marberger, Richie, de la Rosette.

Drafting of the manuscript: Heuer, Gill, Guazzoni, Kirkali, Marberger, Richie, de la Rosette.

Critical revision of the manuscript for important intellectual content: Heuer, Gill, Guazzoni, Kirkali, Marberger, Richie, de la Rosette.

Statistical analysis: Heuer, Gill, Guazzoni, Kirkali, Marberger, Richie, de la Rosette.

Obtaining funding: None.

Administrative, technical, or material support: None.

Supervision: Heuer.

Other (specify): None.

Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.

Funding/Support and role of the sponsor: None.

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Footnotes

a Department of Urology, University Medical Centre, Hamburg-Eppendorf, Germany

b University of Southern California Institute of Urology, Los Angeles, California, USA

c Department of Urology, University Vita-Salute, San Raffaele, Milan, Italy

d Department of Urology, Dokuz Eylul University, School of Medicine, Izmir, Turkey

e Department of Urology, Medical University of Vienna, Vienna, Austria

f Brigham and Women's Hospital, Division of Urology, Boston, Massachusetts, USA

g Department of Urology, AMC University Hospital, Amsterdam, The Netherlands

lowast Corresponding author. Department of Urology, Martinistraße 52, University Medical Centre, 20246 Hamburg-Eppendorf, Germany. Tel. +4940741054462; Fax: +49741059022.

Article information

PII: S0302-2838(09)01027-6
DOI: 10.1016/j.eururo.2009.10.023
© 2009 European Association of Urology. Published by Elsevier B.V.

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