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Keywords:

  • nephron-sparing surgery;
  • small renal mass;
  • repeat;
  • robot-assisted partial nephrectomy

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Objective

  • To demonstrate the feasibility, and to report our single-centre perioperative outcomes of repeat robot-assisted partial nephrectomy (RAPN).

Patients and Methods

  • From June 2006 to June 2012, 490 patients underwent RAPN for a renal mass at our centre. Of these patients, nine who had undergone previous ipsilateral nephron-sparing surgery (NSS) were included in the analysis.
  • Patient charts were reviewed to obtain demographic data, preoperative surgical history, operative details, and postoperative outcomes and follow-up data.

Results

  • In all, 12 tumours were removed in nine patients (median age 69 years; six female). A third of the operations were performed on patients with a solitary kidney. The median (range) R.E.N.A.L. nephrometry score for the resected masses was 7 (4–8).
  • The warm ischaemia time was 17.5 min and in three of the nine patients an unclamped procedure was performed. No intraoperative complications were registered, whereas only two minor complications occurred postoperatively. There were no renal unit losses. All surgical margins were negative.
  • There was no significant difference between mean preoperative and latest postoperative mean estimated glomerular filtration rates (70.5 vs 63.5 mL/min/1.73m2, P > 0.05).
  • At a mean (sd) follow-up of 8.3 (13) months, eight of the nine patients with a pathology diagnosis of malignant neoplasm were alive and free from disease at the latest follow-up.

Conclusion

  • Although technically more demanding, repeat RAPN can be safely and effectively performed in patients presenting with local recurrence after primary NSS for kidney cancer.

Abbreviations
CKD

chronic kidney disease

NSS

nephron-sparing surgery

(RA)(L)PN

(robot-assisted) (laparoscopic) partial nephrectomy

WIT

warm ischaemia time

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Robot-assisted partial nephrectomy (RAPN) is gaining momentum in the field of nephron-sparing surgery (NSS), given the unique features offered by the robotic platform. A steadily increasing number of series have been reported [1], and indications for the procedure have successfully expanded to more challenging patients, e.g. obese [2] and elderly [3], and those with prior abdominal surgery [4], as well to challenging masses, such as hilar lesions [5], large tumours [6], complex lesions [7], and multifocal disease [8, 9].

NSS can be a challenging treatment option to pursue in someone who has undergone a prior NSS and developed a new or recurrent tumour in the same kidney. Although radical nephrectomy has been traditionally considered reasonable in this challenging setting, repeat PN may still be the preferred option, as it maximises preservation of renal function. This is also supported by the concept that most (so-called) recurrences are actually due to multifocality and the bilateral nature of the disease, which further support the role of NSS, if feasible [10].

Repeat open PN has been shown to be associated with good functional and oncological outcomes [11]. However, the procedure can be technically challenging, because of the higher risk of complications. The challenges become even more significant when a minimally invasive NSS technique is planned, e.g. laparoscopic PN (LPN). In a study from our own institution, Turna et al. [12] reported their experience with LPN in patients who had undergone previous ipsilateral procedures, including percutaneous nephrolithotomy and nephrostomy tube placement. In that series, all patients were successfully completed with no need for open conversion, showing that LPN after previous ipsilateral renal surgery is feasible and effective, given adequate laparoscopic experience and careful patient selection.

According to recent comparative analyses [13, 14], RAPN might offer a more attractive minimally invasive NSS technique compared with its standard laparoscopic counterpart. And this proposition may be even more applicable when a repeat PN is indicated. However, there is paucity of published data about the outcomes of RAPN in this setting.

The aim of the present study was to demonstrate the feasibility, and to report our single-centre perioperative outcomes of repeat RAPN.

Patients and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

From June 2006 to June 2012, 490 patients underwent RAPN for a renal mass at our institution. The patient data were prospectively accrued in an Institutional Review Board-approved RAPN registry. Of these patients, nine had undergone previous ipsilateral PN and were included in the present analysis (Fig. 1).

figure

Figure 1. 71-year-old male patient with von Hippel–Landau disease who had previously undergone a laparoscopic PN for two right renal masses. Three months later, the patient underwent a robotic PN for a 2.6 cm left anterior lower pole renal tumour. On follow up imaging two years later, a 2.7 cm homogeneous solid hypovascular enhancing mass in the lateral aspect of the right kidney (RENAL Score = 8x) was detected. Surgical clips and suture material could be seen from Prior PN. Repeat robotic PN was successfully performed, without clamping the hilum.

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Patient charts were reviewed to obtain demographic data, preoperative surgical history, operative details (including warm ischaemia time, WIT), and postoperative outcomes, including pathological findings (including positive margin rate), complications (graded according to the Clavien classification [15]) and follow-up data. Patients were followed at regular intervals with history, physical examination, renal functional tests, and abdominal and chest imaging.

Functional outcomes were assessed with preoperative and postoperative serum creatinine, and estimated GFR (eGFR), calculated according to the Modification of Diet in Renal Disease study equation. Moreover, chronic kidney disease of each patient was defined according to National Kidney Foundation, Kidney Disease Outcomes Quality Initiative. Tumour complexity was graded according to the R.E.N.A.L. nephrometry score [16].

Surgical Technique

The RAPN surgical technique at our institution has been reported previously [17]. Technical modifications specifically related to this patient population are mostly related to the presence of previous abdominal scars, requiring transperitoneal access through the most geographically distant quadrant to minimise the risk of inadvertent intra-abdominal injury. Moreover, meticulous lysis of intra-abdominal adhesions is needed to avoid injury to adjacent organs and avoid significant haemorrhage. If adhesions involving the bowel and its mesentery are present, use of electrocautery should be minimised.

Another problem is represented by the previously dissected renal hilum that requires a specific approach. Dense adhesions around the hilum are expected, and special care is needed to handle fibrous tissue encasing the renal vessels. The first decision is to clamp or not, and hilar clamping should be minimised. Whenever deemed necessary, skeletonising the artery and vein individually can be too risky and not advisable. Thus, en bloc clamping with the use of a Satinsky can be performed, instead of bulldog clamping for individual renal vessels, as currently done for a standard RAPN case.

Moreover, a previously dissected kidney may have the Gerota's mobilised or even excised resulting in tricky re-mobilisation of the kidney. The kidney might be completely lacking of fat and directly adherent to the undersurface of the abdominal wall. This should be remembered during renal mobilisation. Densely adherent perinephric tissue may result in a high likelihood of entering the subcapsular plane, and preventing such stripping of the capsule is of critical importance to facilitate the following surgical step of renorrhaphy. Overall, the limited mobility of the kidney may slow and make tumour excision and renal reconstruction more difficult. Finally, other intraoperative strategies, e.g. hydration, administration of mannitol, and low pneumo-pressure, can be useful aids to minimise surgical impact on renal function.

Descriptive analyses were used to describe the characteristics of the patient samples, expressed as Median (Inter-quartile Range) percentages and frequencies.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

Demographics of the study population are shown in Table 1. In all, 12 tumours were removed in nine patients. The median age of the patients in was 69 years and six of the nine were female. A third of the operations were performed on patients with a solitary kidney. The most common previous ipsilateral NSS procedure was open PN (five patients) and the median time from the previous NSS procedure was 39.4 months. In all patients, the mass was located in a different portion of the previously treated kidney. The median R.E.N.A.L. nephrometry score for the resected masses was 7, anterior position being the most frequent and the median tumour size was2 cm.

Table 1. Demographics of the nine patients included in the study
VariableValue
  1. *Only the largest tumour scored. ASA, American Society of Anesthesiologists; OPN, Open PN; LRFA, laparoscopic radiofrequency ablation.

Total number of tumours12
Median (range): 
Tumours, n1 (1–3)
Age, years69 (61.5–71)
Body mass index, kg/m227.2 (23.8–30.1)
ASA score3 (2–3)
Charlsoncomorbidity score2 (1–4.5)
Time from previous NSS procedure, months39.4 (28.7–81.1)
R.E.N.A.L. nephrometry score*7 (4.5–8)
Tumour size on CT, cm2 (1.5–2.7)
n/N: 
Female gender6/9
Solitary kidney3/9
Type of previous NSS procedure: 
OPN5/9 (55.5)
RAPN2/9
LPN1/9
LRFA1/9
Left side6/9
Position of tumour:* 
Hilar1/9
Anterior4/9
Neither anterior nor posterior2/9
Posterior2/9

Surgical outcomes are detailed in Table 2. The median procedure duration was 153 min, with a median WIT of 17.5 min. In three of the nine patients, an unclamped procedure was used. The median (range) estimated intraoperative blood loss was 150 (75–275) mL. No intraoperative complications were registered, whereas only two minor (Clavien I) complications occurred postoperatively, one ileus and one transient elevation in serum creatinine, not requiring dialysis. There was no loss of renal units and all surgical margins were negative.

Table 2. Surgical outcomes in the nine patients undergoing repeat RAPN
VariableValue
  1. *Clamped patients only. One ileus, one temporary acute renal failure.

Median (range): 
Operating room time, min153 (105–236)
Estimated blood loss, mL150 (75–275)
WIT, min*17.5 (11.5–29.2)
Tumour size on pathology, cm2.3 (1.2–3.6)
Hospital stay, days3 (2–3.5)
n/N: 
Management of renal hilum: 
En bloc clamping with Satinsky4/9
Unclamped3/9
Selective clamping with bulldogs2/9
p Stage: 
T1a7/9
T3a1/9
NA1/9
Histology type: 
Clear cell RCC3/9
Papillary RCC3/9
Chromophobe RCC2/9
Benign cyst1/9
Postoperative complications: 
Total2/9
Clavien Grade I2
Clavien Grade II–IV0

For functional outcomes, there was a mean 7% decrease in eGFR postoperatively, without a significant difference between preoperative and latest postoperative mean eGFR values (70.5 vs 63.5 mL/min/1.73 m2, P > 0.05). Changes in chronic kidney disease (CKD) stages are detailed in Table 3.

Table 3. Changes in CKD stageThumbnail image of

The mean (sd) follow-up was 8.3 (13) months. Of the eight patients with a pathology diagnosis of malignant neoplasm, all were alive and free from disease at the latest follow-up.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References

The overall benefit of NSS in the management of renal tumours is nowadays widely recognised and documented. Postoperative local tumour recurrence in patients who have previously undergone NSS represents a challenging scenario. The incidence of local recurrence after a PN varies between zero and 17% depending on the series [18]. While a rare occurrence for sporadic tumours, recurrence is expected in multifocal and heritable cases.

Management options for recurrent tumours include radical nephrectomy, ablation and repeat PN. Among these, a radical nephrectomy can be regarded as the least appealing because of the potential deleterious effect on renal function. Ablative techniques may not be viable, because of tumour location, despite their demonstrated safety and efficacy in patient populations where need for salvage intervention is common [19].

The present series represents the first to show the feasibility of RAPN for ipsilateral recurrent renal tumours. In all, 12 tumours were removed in nine patients. A third of the operations were performed on patients with a solitary kidney. The most common previous ipsilateral NSS procedure was open PN (five patients) and the median time from the previous NSS procedure was 39.4 months. The median R.E.N.A.L. nephrometry score for the resected masses was 7, anterior position being the most frequent and the median tumour size was 2 cm.

Repeat open PN has been reported sparsely in the literature and mostly in patients with Von Hippel–Lindau disease (Table 4) [11, 12, 20-22].

Table 4. Surgical outcomes of PN after previous ipsilateral kidney surgery: literature overview
ReferenceTechniquePatients (tumours), nPrevious kidney procedureTime from previous surgery, yearsSolitary kidney, % or n/NTumour size, cmOT, hUnclamped, % or n/NType of ischaemiaIschaemia time, minEBL, mLIntraop. complications, %Postop. complications, % or n/NPatients on CHD, n (%)
  1. *Three of the procedures done laparoscopically; one of the procedures done laparoscopically; median values; §mean values; nr, not reported. OPL, open pyelolitotomy; OPN, open PN; OPP, open pyeloplasty; PCNL, percutaneous nephrolithotomy; RB, renal biopsy; OT, operative time; EBL, estimated blood loss; CHD, haemodyalisis.

Turna et al. [12].LPN25 (25)OPL; OPN; OPP; PCNL; RB6.6§02.5§3§0Warm35.8§215§0120
Johnson et al. [11]OPN*47 (51)OPNnr333.57.539.3Warm31180035.343.23 (5.8)
Magera et al. [20].OPN18 (22)OPN3.9671.9nr64Cold or warmnr70019280
Kowalczyk et al. [21].OPN13 (16)RFA2.7503.2nr25Cold27150037500
Liu et al. [22]OPN25OPN8.251003.58.552Cold46240052 3 (12)
Present seriesRAPN9 (12)OPN; RAPN; LPN; LRFA3.283/922.53/9Warm17.515002/90

While the benefits of a repeat PN, such as the improved functional outcomes and avoidance of dialysis, the potential overall survival advantage and the prevention of future imperative NSS on a solitary kidney, are unquestionable, risk and complications have been recognised for open PN procedure [10]. In this regard, the application of robotic technology, and its unique features, can provide the surgeon with an effective tool to address these issues.

Due to the intense perinephric fibrosis, tissue planes in a repeat PN procedure can be obscured, and the surgery can be prolonged. Surgical time for repeat open PN series has approached 7–8 h even in experienced hands [22]. This was not the case in our experience with repeat RAPN, as the operation duration in this specific population was similar to our overall RAPN population [17].

Despite volume loss being recently suggested as the primary determinant of ultimate renal function after PN [23], ischaemia time remains a modifiable factor that should be taken into account [24]. The median WIT was 17.5 min in the present series, which compares favourably with previously reported repeat open PN or LPN series. The relatively long WIT in these series could be attributed to the limited mobility of the previously operated kidney, potentially limiting the suturing angles available to the surgeon and thus slowing the sutured renal reconstruction. The tumour can also be more difficult and slower to excise because of the adherence of the perirenal fat to the renal surface around the tumour. Even if these issues remain for the RAPN technique, it can be speculated that the features offered by the robotic platform facilitate these key steps of the PN procedure, ultimately improving its surgical outcomes.

To minimise the amount of ischaemia, these surgeries are frequently performed without renal hilar clamping, resulting in substantial intraoperative blood loss. An unclamped procedure was used in three of the nine patients in the present series, whereas this was done in 25–64% of cases in open PN series [11, 20-22]. The estimated blood loss associated with these surgeries was found to be over five-times higher than those patients undergoing a routine open PN [11, 22]. Owing to the extended operative times and increased blood loss, patients might frequently need to be closely monitored and their hospital stay is likely to be prolonged [23]. For the present repeat RAPN patients, estimated blood loss (median 150 mL) as well the hospital stay (median 3 days) was also found to be similar to our overall RAPN population [17].

For repeat NSS, the fibrosis from the prior surgery can increase the incidence of intraoperative injury to adjacent structures. Interestingly, one of the initial series from the Mayo Clinic did not report any increased morbidity with repeat open PN [20]. More recent series from the National Cancer Institute have seen more of the anticipated complications with repeat surgery, some of them appearing to be more common with repeat NSS, e.g. pleural injuries and pancreatic leakage [11, 22]. Major renovascular injuries have been reported in up to 25% of patients [22]. Finally, the incidence of urine leak appeared to be about three-times higher than most series. Clearly, number of tumours removed, and the timing of re-intervention may influence the rates and types of complications. There were no intraoperative complications in our present series and only two minor complications occurred postoperatively, one ileus and one temporary increase in serum creatinine, which was managed conservatively, with no need for dialysis.

For functional outcomes, there was a mean 7% decrease in eGFR postoperatively, without a significant difference between preoperative and latest postoperative mean eGFR values (70.5 vs 63.5 mL/min/1.73 m2, P > 0.05). More importantly, there was no loss of renal units and all patients preserved an adequate renal function to prevent renal replacement therapy. Similarly, the functional outcomes of repeat open PN series reported only minimal decline in both serum creatinine and creatinine clearance after surgery [11, 22].

The mean (sd) duration follow-up was 8.3 (13) months. Of the eight patients with a pathology diagnosis of malignant neoplasm, all were alive and free from disease at the latest follow-up. Of course, the limited follow-up period does not allow a reliable assessment of the oncological outcomes. However, the negative surgical margins in all patients represent an encouraging finding.

Other limitations of the present analysis are related to the few patients. Because of this, a comparative analysis with other treatment options for this specific patient population was not done. The main aim of the present study was to provide evidence of the feasibility and the safety of the technique in this setting. Moreover, for the evaluation of kidney function, this should be optimally performed, especially for patients with two functioning kidney units, by using renal scan, which was not available for the present study population. Moreover, the duration of follow-up represents another significant limitation of the present analysis.

In conclusion, repeat RAPN can be offered to patients presenting with local recurrence after primary NSS for localised RCC. Although technically more demanding, repeat PN can be safely and effectively performed in a minimally invasive fashion with the aid of robotic technology in this subset of patients.

Larger studies with longer follow-ups are needed to provide further evidence of the outcomes of this challenging procedure.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Conflict of Interest
  8. References
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