Robot-assisted partial nephrectomy for sporadic ipsilateral multifocal renal tumours

Authors

  • Humberto Laydner,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Riccardo Autorino,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Gregory Spana,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Fatih Altunrende,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Bo Yang,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Rakesh Khanna,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Michael A. White,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Wahib Isac,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Shahab Hillyer,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Georges-Pascal Haber,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Robert J. Stein,

    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
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  • Jihad H. Kaouk

    Corresponding author
    1. Center for Laparoscopic and Robotic Surgery, Glickman Urological and Kidney Institute Cleveland Clinic Foundation, Cleveland, OH, USA
      Jihad Kaouk, Zegarac Pollock Professor of Surgery, Director of the Laparoscopic & Robotic Surgery Institute, Vice Chair for Surgical Innovations, Cleveland Clinic, 9500 Euclid Avenue, Glickman Urology and Kidney Institute/Q10-1, Cleveland Clinic, Cleveland, OH, 44195, USA. e-mail: kaoukj@ccf.org
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Jihad Kaouk, Zegarac Pollock Professor of Surgery, Director of the Laparoscopic & Robotic Surgery Institute, Vice Chair for Surgical Innovations, Cleveland Clinic, 9500 Euclid Avenue, Glickman Urology and Kidney Institute/Q10-1, Cleveland Clinic, Cleveland, OH, 44195, USA. e-mail: kaoukj@ccf.org

Abstract

Study Type – Therapy (case series)

Level of Evidence 4

What’s known on the subject? and What does the study add?

Although laparoscopic excision of ipsllateral multifocal renal tumours is feasible, the average warm ischemia time is prolonged. Robotic partial nephrectomy in this subset of patients using blunt dissection to enucleate the tumour is feasible and safe.

This study demonstrates further that robot-assisted partial nephrectomy with a small margin of normal tissue is feasible and safe with an acceptable range of warm ischemia time in patients with sporadic ipsilateral multifocal renal tumours. This study also suggest that robotic partial nephrectomy for this particular group of patients may better preserve renal function compared to laparoscopic approach, however this needs to be confirmed with prospective comparative studies.

OBJECTIVE

• To report our short-term results of robot-assisted partial nephrectomy for treating sporadic multiple ipsilateral renal tumours.

METHODS

• Over a 3-year period, eight patients with two or more ipsilateral renal masses underwent nine robotic partial nephrectomies in our institution.

• We evaluated the PADUA and R.E.N.A.L. nephrometry scores, intraoperative outcomes, histopathological characteristics, complications according to Clavien classification and renal function outcomes.

RESULTS

• In total, 19 tumours were removed from eight patients in nine procedures. Mean operative time was 199 ± 47 min (median 200; range 150–300). Mean size of the dominant lesion was 3.0 ± 1.1 cm (2.7; 1.6–4.8) and overall mean tumour size was 2.2 ± 1.2 cm (1.9; 0.4–4.8). Mean number of tumours removed per patient was 2.4.

• Median PADUA and R.E.N.A.L. scores were 7 and 6 (with the predominance of an anterior, non-hilar position), respectively.

• Excluding the six off-clamp resected tumours, the mean warm ischaemia time was 21 ± 9.2 min (21; 10–35). Mean estimated blood loss was 250 ± 154 mL (200; 100–500) and no patient required transfusion. There were no intraoperative complications or conversion to open surgery. One patient had atrial fibrillation, resolved with anti-arrhythmic drugs. Mean length of stay was 4.2 ± 0.97 days.

• Sixteen of the nineteen tumours were malignant, most of papillary type and Fuhrman grade II.

• The mean decrease in glomerular filtration rate was 4%, with a mean follow-up of 14 months.

CONCLUSIONS

• Robotic partial nephrectomy for sporadic ipsilateral multifocal renal tumours is feasible and safe.

• Off-clamp resection of multiple tumours can also be safely performed in carefully selected lesions.

Abbreviations
RPN

robot-assisted partial nephrectomy

GFR

glomerular filtration rate.

INTRODUCTION

Multifocality of renal cell carcinoma can be defined by the presence of two or more tumoral foci in the same kidney, separated by a strip of normal tissue [1]. The incidence of multifocal renal tumours ranges between 4.3 and 25% in previous series [2]. Since its development, nephron sparing surgery has increasingly gained acceptance, showing oncological outcomes similar to radical nephrectomy [3]. Currently it is considered in many major guidelines as the primary treatment modality in the management of small (T1a) renal tumours [4,5]. There is also evidence supporting the use of nephron sparing surgery for T1b lesions [6]. Since the first robot-assisted partial nephrectomy (RPN) was described in 2004 [7], there has been an exponential growth of RPNs reported in the literature. The advantages of the endo-wrist coupled with increasing surgeon experience have led to the use of RPN for complex cases. Rogers et al. [8] were the first to report RPN in the setting of multiple renal tumours and hereditary kidney cancer.

Herein we describe our experience with RPN for patients with two or more ipsilateral tumours by reporting surgical technique and outcomes.

PATIENTS AND METHODS

We reviewed our Institution Review Board approved database and charts of eight consecutive patients with ipsilateral multifocal kidney tumours who underwent RPN at our institution between April 2007 and July 2010. We reviewed data from imaging, operative, anaesthesiology and pathology reports, as well as from the discharge and laboratory records. Glomerular filtration rate (GFR) was calculated using the abbreviated Modification of Diet in Renal Disease study equation, GFR in mL/min/1.73 m2= 186 × (serum creatinine)−1.154× age−0.203× (0.742 if female) × (1.210 if African American) [9]. Complications were evaluated using the Clavien classification [10]. The PADUA [11] and R.E.N.A.L. [12] nephrometry scores were applied to each of the 19 tumours.

All patients were placed in the modified flank position at approximately 60 degrees, with the table flexed and in slight Trendelenburg. The abdomen was insufflated to 15 mmHg with a Veress needle at the lateral border of the rectus at the level of the twelfth rib and this served as the 12-mm camera port. An 8-mm port was placed at the lateral border of the ipsilateral rectus muscle, about 3 cm below the costal margin. A second 8-mm port was placed about 5–7 cm cephalad to the anterior superior iliac spine. An assistant 12-mm port was placed along the lateral border of the rectus muscle in the lower abdominal quadrant. For right-sided cases, a 5-mm port was placed in the sub-xiphoid area for liver retraction (Fig. 1). The robot was then positioned over the patient’s shoulder with the camera oriented in line with the kidney. A 30-degree down-scope was used along with the pro-grasp robotic grasper in the left arm for retraction and either the monopolar scissors or hook in the right arm. The fourth robotic arm was not used. The colon was reflected medially and the dissection continued cephalad to mobilize the spleen or liver. Dissection was taken along the psoas muscle with anterior elevation of the ureter and gonadal vein to identify the renal hilum. The hilum was cleared and renal vessels were dissected to allow for occlusion with bulldog or Satinsky clamps. Gerota’s fascia was opened and dissection was carried out along the renal capsule until the mass was exposed. The fat was then cleared circumferentially around the mass, allowing for visualization of at least 1–2 cm of normal parenchyma for renal reconstruction. All attempts were made to leave the overlying Gerota’s fascia atop the mass to assist in histopathological staging and also to use as a handle for retraction. The laparoscopic ultrasound probe was used to plan excision margins. The renal capsule was scored to delineate the boundaries of resection. Before hilar occlusion, 12.5 g mannitol was given intravenously. Usually, the artery and vein were both clamped individually with bulldog clamps. However, if the hilum had a complex anatomy with multiple branches, or if for any reason the hilar dissection was exceedingly difficult, a Satinsky clamp was used and the hilum was then clamped en bloc. Tumours that were mostly exophytic with minimal cortical involvement were resected without hilar clamping, using hem-o-lok clips (Teleflex Medical, Research Triangle Park, NC, USA) to control bleeding vessels from the parenchyma. The tumour was resected along the previously scored margin using cold scissors and the bedside assistant used suction to clear the resection bed and allow for improved visualization while applying slight counter-retraction as needed (Fig. 2). If multiple tumours were close enough to have an intersection between their resection margins, they were resected together en bloc. A 2-0 polyglatin suture with a knot and hem-o-lok clip fixed to the free end was used as a running suture of the tumour excision bed to achieve haemostasis and closure of the collecting system. The hilum was unclamped and the renal excision bed was inspected for haemostasis. The renal parenchymal defect was approximated using 0 polyglatin sutures. The defect was covered with oxidized cellulose (Surgicel; Johnson and Johnson, Somerville, NJ, USA) and a fibrin sealant (Evicel; Johnson and Johnson or Vitagel; Orthovita, Malvern, PA, USA). The specimen was placed in a laparoscopic entrapment sac and removed from a lower quadrant port site. All 12-mm incisions were closed with a 0 polyglatin suture using the Carter–Thomason device (CooperSurgical, Trumbull, CT, USA). A Jackson–Pratt drain was placed through a lower lateral port.

Figure 1.

Positioning of the trocars for right (A) and left (B) robotic partial nephrectomy.

Figure 2.

Tumour resection.

RESULTS

Eight patients were submitted to nine procedures (one patient underwent bilateral RPN) and had a total of 19 tumours removed. Patients’ preoperative characteristics are listed in Table 1. Seventy-five percent of the patients were men and mean patient age was 67 ± 11 years (median 69; range 44–83). Genetic testing was performed if the patient and some consanguineous relative had any clinical suspicion of Von Hippel–Lindau disease (one patient, with negative result).

Table 1.  Patient demographics and tumour characteristics
PreoperativeHistopathological
PatientGenderAgeASABMISideTumour no.Size (cm)PADUAR.E.N.A.L.Histological subtypeGrade*Parenchymal marginpT
  • *

    Fuhrman nuclear grading system,

  • †papillary and clear cell features,

  • papillary architecture with foci of the papilla lined by clear cells. ASA, American Society of Anesthesiologists score; BMI, body mass index; PADUA [11] and R.E.N.A.L. [12]: renal tumour scores based on preoperative imaging.

1M68227R12.677aPapillary3Negative1a
L22.47Papillary3Negative1a
12.775aPapillary2Negative1a
21.28Papillary2Negative1a
31.864pPapillary2Negative1a
2F44228R11.686aAngiomyolipomaNegative
20.464aAngiomyolipomaNegative
3F74329R11.996pClear cell2Negative1a
21.499ahClear cell2Negative1a
4M74326L13.576pPapillary2–3Negative1a
21.288ahUnclassified2–3Negative1a
5M83325R14.886aPapillary3Negative1b
21.57Papillary3Negative3a
6M61327R13.57Papillary2Negative1a
21.087aPapillary2Negative1a
7M66229R12.064aPapillary2Negative1a
21.075aPapillary3Negative1a
8M69223L14.587aAngiomyolipomaNegative
22.097aPapillary3Negative3a

Twelve masses were on the right side in six patients and seven masses were on the left side in three patients. Mean operative time was 199 ± 47 min (200; 150–300). All patients had at least two or more tumours removed (Fig. 3). Mean size of the dominant lesion was 3.0 ± 1.1 cm (2.7; 1.6–4.8) and overall mean tumour size was 2.2 ± 1.2 cm (1.9; 0.4–4.8). Table 1 also lists tumour side, number, size, nephrometry scores and histopathological characteristics.

Figure 3.

Preoperative (A) and postoperative (B) computed tomography scan of patient 6.

Six of 19 tumours did not require hilar clamping. Excluding the off-clamp procedures, mean warm ischaemia time was 21 ± 9.2 min (21; 10–35). Mean estimated blood loss was 250 ± 154 mL (200; 100–500) and no patient required blood transfusion. There were no intraoperative complications and no conversion to pure laparoscopic or open surgery.

In the postoperative period, one case of atrial fibrillation was successfully managed with anti-arrhythmic drugs. The patient did not require to be transferred to the intensive-care unit and was discharged home on the fifth postoperative day. Mean length of stay was 4.2 ± 1.0 days (5; 3–5). Table 2 lists intraoperative and postoperative outcomes.

Table 2.  Outcomes
IntraoperativePostoperative
PatientNo. of tumoursOperative timeClamp typeWIT (min)EBL (mL)PRBC TransfusionComplicationsLOS (days)
  • *

    Grade II according to Clavien classification. WIT, warm ischaemia time; EBL, estimated blood loss; PRBC, packed red blood cells; LOS, length of stay.

1        
 R2209Satinsky3530005
 L3232Offclamp050005
22153Bulldog2110003
32204Satinsky1520003
Offclamp0
42150Bulldog321500atrial fibrillation*5
52300Offclamp010003
62160Bulldog + Satinsky1550005
72200Satinsky1020005
82180Bulldog2220004

Mean follow-up was 14 months. Of the 19 resected tumours, 16 were RCCs on final histopathological reports. All tumours had negative margins. The GFR was decreased by an average of 4%. Table 3 details renal function outcomes.

Table 3.  Renal function
PatientPreoperative creatinine (mg/dL)6-month postoperative creatinine (mg/dL)Preoperative eGFR (mL/min/1.73 m2)6-month postoperative eGFR (mL/min/1.73 m2)Variation of eGFR (%)
  1. eGFR, estimated glomerular filtration rate.

1     
 R0.961.0982.871.5−11.3
 L1.271.3159.857.7−2.1
20.741.0490.699.9+9.3
30.790.8891.580.8−10.7
41.121.1968.163.5−4.6
51.641.4642.949+6.1
61.191.1666.168+1.9
71.281.945937−22
80.770.78105104.90

DISCUSSION

In patients with RCC, multifocality is detected in up to 25% of the cases after histopathological examinations [2]. Authors have found no statistically significant differences in cancer-specific survival between patients with multiple ipsilateral renal tumours treated by radical nephrectomy or nephron sparing surgery [13,14]. Long-term local recurrence rates and metastasis-free survival after partial nephrectomy for RCC have been shown to be very low and equivalent to radical nephrectomy for tumours of 7 cm or smaller [15,16].

The association between papillary renal tumours and multifocality has been shown previously [17]. Recently, Tsivian et al. [2] found that occult multifocal RCC was more commonly associated with male gender, lesions between 2–4 cm, family history of RCC, histological subtype other than clear cell (specially papillary), and Fuhrman grade IV. In our series, 13 of the 19 tumours (16 RCCs) were papillary, six of the patients were male, the dominant lesion measured 2–4 cm in six of the nine procedures, and none of the patients had Fuhrman grade IV tumours or family history of RCC.

Another major concern of partial nephrectomies in general, and particularly in the setting of multifocality, is the potential damage to renal function caused by transient ischaemia of the kidney. Lane et al. [18] after analysing the data of 1169 patients undergoing partial nephrectomy, showed that the major predictor of a postoperative decreased renal function is a low baseline GFR and that ischaemia time is the greatest modifiable risk factor. They also encourage the preoperative evaluation of GFR rather than serum creatinine alone, because up to 25% of patients with a normal serum creatinine have a GFR <60 mL/min/1.73 m2, which configures moderate chronic kidney disease. Generally, 30 min of warm ischaemia time has been considered to be safe and cold ischaemia has been recommended when a longer time is expected [19]. We had a favourable mean warm ischaemia time in comparison to other series for multiple tumours [20–22], with similar renal function outcomes. Table 4 displays data of previous series of laparoscopic and robotic partial nephrectomy for multifocal renal tumours. The mean warm ischaemia time of the robotic series is 15 min shorter than the laparoscopic counterpart. The mean percentage decrease in GFR is also lower in robotic series. This is a particularly challenging subgroup of patients, so we hypothesize that the easier dissecting, cutting and suturing manoeuvres allowed by the robot endowrists could possibly have a role in these findings.

Table 4.  Published laparoscopic and robot-assisted partial nephrectomies for ipsilateral multifocal renal tumours
 Type of surgeryNo. of patientsNo. of tumours/ patientMean tumour size (cm)Mean operative time (min)Mean WIT (min)Mean EBL (mL)No. of patients requiring transfusionConversionPostoperative complicationsMean % decrease in eGFRMean LOS (days)
  • *

    Mean increase in serum creatinine of 10%. LPN, laparoscopic partial nephrectomy; RPN, robot-assisted partial nephrectomy; WIT, warm ischaemia time (excluding the off-clamp resections); EBL, estimated blood loss; HALS, hand-assisted laparoscopic surgery; eGFR, estimated glomerular filtration rate; LOS, length of stay, NS, not stated.

Flum and Wolf [20] 2010LPN72.32.12024238611 (HALS)0NS*2.3
Lin et al. [22] 2008LPN1422.928137.320010323.53.7
Total LPNLPN212.152.524139.629321323.53
Boris et al. [21] 2009RPN102.72.325726.736001 (open)15.34
PresentRPN82.42.219921.42500013.74.2
Total RPNRPN182.52.25228243050124.54.1

Huber et al. [23] evaluated bleeding complications after open nephron sparing surgery in 196 consecutive cases. They used as a criterion for haemorrhage a persistent decreasing haematocrit that could not be accounted for by intraoperative blood loss, requiring the transfusion of at least two units of blood. They identified multifocality and imperative indication as risk factors for haemorrhage. We did not have any haemorrhage complications in our series.

In the present series, the median PADUA score was 7. Ten tumours were scored as 6 or 7, nine tumours as 8 or 9, and no tumour scored 10 or higher. With the R.E.N.A.L. score, 12 tumours were classified as 4 to 6, seven tumours as 7 to 9, and no tumour as 10 to 12. Tumours were anterior, posterior and lateral in 12, three and four cases, respectively. Two tumours were hilar. Given our relatively small sample, we did not attempt any correlation between scores and outcomes. However, an increasing number of reports are showing a significant correlation of these scores with intraoperative and postoperative outcomes, such as warm ischaemia time, estimated blood loss, length of stay [24], risk of urine leak [25] and overall complications [11]. These studies highlight the importance of quantifying tumour complexity.

Some authors have published their experience with RPN for multiple tumours along with their overall results and did not state the individual outcomes for multifocal tumour procedures [26–29]. Before the present study, there was only one series focused specifically on RPN for multiple renal tumours [21]. Generally, our outcomes were similar to what they found. However, there are two major differences between the studies. The first is related to the patients’ characteristics. While 70% of the patients reported by Boris et al. [21] had a known hereditary renal cancer syndrome, in our series all the patients had multifocal tumours without a known genetic cause. The second major difference regards the tumour resection technique. We performed sharp resection along a previously scored small margin of tissue. In Boris et al.’s study [21], the robot was used to reproduce a method previously described by the same institution for open parenchymal sparing surgery in patients with multiple hereditary renal tumours [30]. The method consists of blunt dissection of the tumour from the parenchyma, enucleating the mass. Their follow-up, like ours, is still too short to evaluate recurrence. It would not be surprising if their cohort had a higher recurrence in the future because patients with hereditary RCC are expected to have rates of local recurrence as high as 35%[31]. Our study shows that it is feasible to perform sharp resection of sporadic multifocal tumours without incurring unacceptable ischaemic times. Moreover, the mean decrease in GFR observed in our series is within the range observed in the literature. In an attempt to minimize ischaemic damage, we usually start excising exophytic tumours off-clamp, and then proceed to deeper tumours with the hilar vessels clamped.

Although our study was based on a prospectively collected database, it is a retrospective analysis. Other limitations of this series include a relatively small sample, a short follow-up period and the absence of a control group for comparison. Also, most of our patients had only two lesions, and these results may not be simply extrapolated to patients with more tumours. Finally, our data represent the outcomes from a single high-volume centre with extensive experience in minimally invasive surgery, particularly RPN, and they may not necessarily be reproducible in less experienced centres.

In the short-term evaluation of this complex subset of patients, RPN for multifocal sporadic ipsilateral tumours was shown to be feasible, with safe ischaemia time. Off-clamp procedures are also feasible and safe for appropriately selected tumours. Complication rates are not different from those generally found in the literature.

CONFLICT OF INTEREST

Jihad H. Kaouk and Georges-Pascal Haber are Speakers, and Consultants for Intuitive Surgical.

Ancillary