European Urology

1. Introduction

Partial nephrectomy for small renal tumours provides equivalent long-term oncologic results to radical nephrectomy with the advantage of preservation of renal function [1]. In the hands of a skilled laparoscopist, laparoscopic partial nephrectomy (LPN) is a safe, effective minimally invasive procedure during which the techniques of open surgery can be replicated with the added inherent advantages of the laparoscopic approach [2]. As in the open procedure, clamping of the renal artery is required during LPN to reduce blood loss and to provide a bloodless field during excision of the tumour, enabling accurate visualisation of the tumour and its safe resection [3], and [4]. However, LPN may be associated with an increased risk of impairment of ipsilateral renal function owing to ischaemic damage during warm ischaemia time (WIT) [2], and currently available minimally invasive renal cooling techniques are cumbersome. In this study we investigated whether WIT could be minimised without compromising other perioperative variables using a modified surgical technique during LPN.

2. Material and methods

Between March 2003 and December 2005, 40 consecutive LPNs, (without selection), were performed by one experienced laparoscopist (H.B.). This surgeon had extensive laparoscopic experience and had performed many LPNs and over 400 laparoscopic procedures in total, precluding a learning curve effect in this study. The LPNs were performed via a transperitoneal approach, except when the tumour was posteriorly situated (6 cases); in these cases the retroperitoneal approach was preferred. In all cases the renal pedicle was dissected, and a rubber sling placed around the renal artery and vein. The kidney was dissected free from the perinephric fat, except for that component in contact with the tumour, and the renal artery was then clamped with a bulldog clip. The renal tumour was excised with cold scissors.

For the first 20 consecutive patients (control group), the collecting system was closed and haemostasis performed with the use of interrupted 2-0 Vicryl sutures (half-circle 31-mm needle for small tumours or half-circle 36-mm needle for larger defects). Tissue adhesive was placed on the tumour bed, and the renal parenchyma then closed with a further 1 Vicryl (half-circle 40-mm needle) interrupted suture over a Surgicel (Ethicon, Somerville, NJ, USA) bolster before unclamping the renal artery. In the subsequent 20 consecutive patients (group 1), the collecting system was closed and the haemostasis was performed by using two separate continuous 2-0 Vicryl sutures (using the needles described above) on the tumour bed (Fig. 1). Knots were performed intracorporaly without using devices such as Lapra-Tys (Ethicon, Somerville, NJ, USA). The bulldog clamp was then removed. For the first 10 of these cases (group 1a), the bulldog clamp was removed from the renal artery after both sutures had been placed. For the subsequent 10 cases (group 1b), the bulldog clamp was removed after the first suture had been placed, and the second running suture was performed on the kidney unclamped (Fig. 2). Additional interrupted sutures were placed if active bleeding was seen after unclamping of the artery, before parenchyma closure. Tissue adhesive (FloSeal*; Baxter Healthcare Corp, Fremont, CA, USA) was then applied to the tumour bed, and the renal parenchyma closed using interrupted 1 Vicryl sutures over a surgical bolster (Fig. 2).

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Fig. 1 Schematic diagram showing steps of operative technique in group 1a. (1) Tumour excision, (2) first running suture on the tumour bed, (3) unclamping of the renal artery, (4) second haemostatic running suture, (5) tissue adhesive application, (6) parenchyma closure over a Surgicel bolster.

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Fig. 2 (1) Upper pole partial nephrectomy, for a 3-cm tumour, using cold scissors. (2) First 2-0 Vicryl running suture to close the collecting system and achieve haemostasis in the same time. (3) Removal of the bulldog clamp, in this case after 10 min of warm ischaemia time. (4) Second 2-0 Vicryl running suture to improve haemostasis on the vascularised kidney. Note the slight bleeding during this step. In this case estimated blood loss was 100 cc. If necessary, extra sutures can be applied to visibly bleeding vessels before parenchyma closure. (5) FloSeal* is applied to improve haemostasis. (6) Closure of the parenchyma over a surgical bolster.

The warm ischaemia time (measured between clamping and unclamping of the renal artery), intraoperative blood loss, serum haemoglobin concentration (measured the day after surgery), operative time, length of hospitalisation, transfusion requirement, and tumour size and margin status were prospectively recorded and compared between the control group and group 1. Similar parameters were compared between groups 1a and 1b.

All statistical comparisons were done with the use of the Student t test, except for nonparametric data, which were compared with the use of the Mann-Whitney U test.

3. Results

All LPNs were performed successfully without conversion to an open procedure. There was no significant difference in mean age, body mass index, or preoperative serum creatinine between the two groups of patients (Table 1). There were no significant difference in blood loss, operative time, and hospitalisation period between the two groups; however, the WIT was significantly shorter in group 1 compared with controls (Table 2), despite the mean tumour size being significantly greater (Table 3). In one patient in group 1, haeminephrectomy was performed with a WIT of 17 min with no bleeding complications. The longest WIT recorded was 22 min during excision of a hilar tumour. There was no significant change in the mean pre- and postoperative serum creatinine level in either groups (Table 1). The incidence of malignancy and size of the surgical margin were not significantly different between the two groups (Table 3). All histologic specimens had negative surgical margins. Pathologic results of each group are summarised in Table 4. The decrease in haemoglobin after operation was significantly higher in the control group (Table 2).

There were no significant difference between the mean operative time, blood loss, or serum haemoglobin concentration reduction between groups 1a and 1b; however, the mean WIT was significantly shorter (ie, 10.3 vs. 16.8 min) in group 1b when the bull dog clamp was removed after only one running suture (Table 5). There were no major perioperative complications. Thirty percent of patients (6 of 20) had a postoperative complication in the control group and 25% in the group 1 (Table 6). Major complications (ie, complications that could not be managed by a pharmacologic treatment) were more frequent in the control group (15% vs. 0%). One elderly patient with multiple comorbidities in the control group developed an intraperitoneal urinary fistula, which was managed initially by a ureteric catheter, but continued problems led to nephrectomy.

4. Discussion

Laparoscopic partial nephrectomy is associated with reduced blood loss, lower analgesia requirement, and convalescent time, but leads to a longer period of warm ischaemia when compared with the open technique [2]. Although some teams have performed LPN without clamping the pedicle in an attempt to minimise WIT, Guillonneau et al [3] and Nadu et al [4] showed that blood loss, perioperative morbidity, and the chances of complete tumour resection were optimised when the renal artery was temporarily controlled.

There are incomplete data regarding the maximum WIT compatible with preservation of renal function; however, 30 min is historically the generally accepted limit based on studies in the 1970s [5]. The safety of this limit in humans is supported by analysis of a series of LPN after which dimercaptosuccinic acid scans performed showed no loss of renal function [4], [6], and [7]. Functional recovery appears to occur within hours after 20 min of warm ischaemia and days after 30 min, and may take several weeks after 60 min of clamping [8]. Recently, Yossepowitch et al [9] found that, although early changes in estimated glomerular filtration rate (GFR) were significantly influenced by cold ischaemia time, with some patients requiring temporary dialysis, cold ischaemia time was not associated with changes in GFR 1 yr postoperatively. Minimisation of WIT therefore is likely to be most important in patients with preexisting renal impairment, or in those with cardiovascular disease when optimal postoperative renal function confers an advantage.

To achieve resection of the tumour and closure of the renal parenchyma with haemostasis within 30 min during LPN requires a strong laparoscopic technique, as shown by large series of LPN in which the mean WIT ranged between 22 and 29 min [2], [4], and [6]. Even in centres of excellence, the WIT is likely to be greater than 30 min during the resection of large, centrally located or multiple tumours, or in unfavourable surgical conditions [10], [11], and [12].

Several techniques of regional hypothermia during LPN have been used including renal artery perfusion with cold physiologic solution, but this technique requires preoperative placement of an angiocatheter [13] and irrigation using a retrogradely placed ureteric catheter [14]. The renal temperatures achieved were between 20 °C to 25 °C, which may not be low enough. Recently, Gill et al [15] described the use of an endobag filled with ice slush. This technique achieved renal parenchymal temperatures of between 5 °C to 19 °C, but prolonged the operation and may interfere with tumour excision. To reduce the WIT, some authors [16] recommend the use of Lapra-Tys to avoid knotting during LPN; however, this technique allows only a moderate reduction of WIT and can lead to a morbidity of its own [17]. One group has reported mean WIT of 21 min using tissue sealant only for haemostasis, although the harmonic scalpel in some cases performed tumour resection, and re-resection was required in 10% [18].

The standard technique for LPN is for the renal pedicle to remain clamped until complete closure of the renal parenchyma, which involves a deep layer of sutures, injection of surgical sealant, and closure of the parenchyma over a bolster. The present study suggests that WIT during LPN could be significantly reduced with no loss of haemostasis or increase in complications by unclamping the renal artery after placing one or two continuous sutures on the tumour bed.

There were fewer complications with the modified technique compared with controls, and those that occurred were less severe. In the control group the interrupted sutures were probably less effective than a continuous suture, explaining the urinary fistula and pseudoaneurysm and arteriovenous fistulas that occurred. Early arterial unclamping also allowed sutures to be applied to visibly bleeding vessels before parenchyma closure. This targeted haemostasis could not be performed with the use of the conventional closure technique. Although no significant difference in blood loss was observed when using either one or two running sutures, we recommend two when the tumour is larger than 3 cm or when the surgeon is not confident with the sutures before unclamping of the artery.

The principle advantage of the adapted renal closure technique is that it enabled significantly more time to be taken during tumour resection and kidney reconstruction, which could be helpful during the LPN learning curve. However LPN remains one of the most challenging laparoscopic procedures, and suturing skills must be perfectly mastered to use this technique.

5. Conclusions

The modified renal closure technique (Baumert's technique) described was effective in maintaining haemostasis and allowed a significant reduction of warm ischaemia, without increasing perioperative morbidity during LPN.

Conflicts of interest

The authors have nothing to disclose.