e u r o p e a n u r o l o g y 5 2 ( 2 0 0 7 ) 1 3 4 0 – 1 3 4 6

Surgery in Motion

Laparoscopic Partial Nephrectomy with Clamping of theRenal Parenchyma: Initial Experience

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Gregory Verhoest a, Andrea Manunta a, Karim Bensalah a, Sebastien Vincendeau a,Nathalie Rioux-Leclercq b, Francois Guille a, Jean-Jacques Patard a,*aDepartment of Urology, Rennes University Hospital, Rennes Cedex, FrancebDepartment of Pathology, Rennes University Hospital, Rennes Cedex, France

Article info

Article history:Accepted April 24, 2007Published online ahead ofprint on May 4, 2007

Keywords:HaemostasisKidney cancerLaparoscopyNephron-sparing surgeryRenal cell carcinoma

Abstract

Objectives: Partial nephrectomy by laparoscopy offers patients conser-vative surgery and a mini-invasive approach; however, clamping of therenal pedicle and the induced warm ischaemia can damage the renalparenchyma. We present a technique of laparoscopic partial nephrec-tomy with haemostasis obtained by clamping of the renal parenchyma.Methods: The procedure was performed by an intraperitoneal or a retro-peritoneal approach. After a working space is created by pneumodissec-tion, Gerota’s fascia is incised and the kidney convexity is dissected. Anendoscopic Satinsky clamp is inserted percutaneously through a 1-cmincision. The renal parenchyma is clamped and the tumour is excised ina bloodless field. The cut renal parenchyma is coated with biologic glue.Results: Five patients with elective indications were operated. Mean agewas 67.8 yr and mean tumour diameter 3.06 cm. One lesion was locatedat the upper pole and four at the lower pole. Mean preoperative serumcreatinine level was 10.9 mg/l. Postoperative serum creatinine level wasunchanged. Mean operative time was 238 min. There was no conversion.Mean blood loss was 250 ml; no transfusions were necessary. The col-lecting duct system was repaired in one patient. No complication wasnoticed. Resection margins were tumour free in all cases. Final patho-logic examination revealed clear cell carcinoma in three cases andangiomyolipoma and oncocytoma in one case each.Conclusion: Laparoscopic partial nephrectomy with clamping of therenal parenchyma can be performed in selected patients with periph-erally placed tumours. The procedure avoids warm ischaemia of thenormal parenchyma while allowing the surgeon to operate in an almostbloodless field. This initial experience in five patients should be validatedin a larger series.# 2007 European Association of Urology. Published by Elsevier B.V. All rights reserved.

* Corresponding author. Department of Urology, Rennes University Hospital,35033 Rennes Cedex, France. Tel. +33 2 99 28 42 70; Fax: +33 2 99 28 41 13.E-mail address: jean-jacques.patard@univ-rennes1.fr (J.-J. Patard).

0302-2838/$ – see back matter # 2007 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.eururo.2007.04.072

Fig. 1 – Peripheral lesion of the left kidney at computed

tomography scan.

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1. Introduction

Over the past two decades, partial nephrectomy hasprogressively gained ground in the management ofsmall renal tumours, providing excellent oncologicresults [1]. Since its first description in 1993 byWinfield [2], the laparoscopic approach has becomean attractive alternative to open surgery [3], butremains a difficult procedure that must be realisedby experienced laparoscopists. The technique hasbeen developed and standardised for both transper-itoneal and retroperitoneal approaches [4,5] andappears reproducible among different surgeonsexperienced in laparoscopic procedures [6].

Tumour location also appears to be a predictivefactor for intraoperative and postoperative compli-cations, with longer warm ischaemia times andhigher rates of urine leakage and postoperativehaemorrhage in central or hilar tumours [7,8].Peripheral tumours are less technically demandingcompared to hilar tumours but are still potentially atrisk. Clamping of the renal pedicle during tumourexcision allows easier control of bleeding [4–9],but the induced warm ischaemia can irreversiblydamage the renal parenchyma. Clamping exclu-sively the involved renal parenchyma seems to be agood alternative when technically feasible. Themain objective of this study is to prove thatparenchymal clamping can be performed by laparos-copy and appears as on option to avoid pedicularclamping and warm ischaemia of the wholekidney.

This article is based on the video ‘‘LaparoscopicPartial Nephrectomy with Clamping of the RenalParenchyma.’’ We present the technique in twopatients, via an intraperitoneal approach in the firstpatient with a lower pole tumour and a transper-itoneal approach in the second patient who had alesion of the upper pole. Additionally, we show ourprimary results through five patients in whom thisprocedure was used.

Fig. 2 – Tumour at the upper pole of the left kidney on

computed tomography scan.

2. Methods

We separately describe the procedure for the intraperitoneal

and for the retroperitoneal approach. Five selected patients

were included in this study, presenting elective surgery for

lesions of the lower or upper pole, or the convexity of the

kidney (Figs. 1 and 2). Patients with imperative indication

(tumour in a single kidney or with overall decreased renal

function) were excluded. All operations were performed by a

single surgeon experienced in urologic laparoscopy. The

choice of the laparoscopic approach was dictated by the

location of the mass and the surgeon’s assessment. No

ureteral catheter was inserted previously. The tumour was

removed with an endoscopic bag. Frozen section analysis was

performed during each procedure.

2.1. Retroperitoneal approach

The patient is placed in a strict flank position with the lower

limbs lowered. A short incision is made under the 12th rib, and

the extraperitoneal space is carefully dissected with the index

finger. After CO2 insufflation, three trocars are introduced

under endoscopic control, as previously described by other

teams [4,5]. The plane anterior to the psoas muscle is

developed. Gerota’s fascia is incised and the kidney is

completely dissected off the perinephric fat, so that it can

Fig. 3 – Introduction of the Satinsky clamp through the

abdominal wall.

Fig. 4 – The Satinsky clamp is placed at distance from the

tumour edge.

Fig. 5 – The parenchyma is clamped and appears

ischaemic.

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be totally mobilised. The lesion is identified; in lower pole

lesions, the ureter is identified prior to tumour excision.

A short incision is then performed under the 12th rib to

introduce a laparoscopic Satinsky clamp (Xomed Micro

France, reference CEVA 103) directly through the abdominal

wall (Fig. 3).

2.2. Transperitoneal approach

The patient is placed in the flank position. Four trocars are

used for this technique and placed as classically described

[4,5]. The colon and the bowels are mobilised. The perirenal fat

is dissected, so that the kidney can be totally mobilised and the

tumour easily accessible. The renal pedicle is gently dissected

but not clamped. If necessary, a tape can be used to correctly

expose the lesion and place the clamp. The tape is passed

around the upper or lower pole of the kidney. The two tape

ends are grasped with endoscopic forceps and downward

traction on the tape tilts the kidney, so that the pole directly

faces the operator and can be easily clamped. A short incision

under the 12th rib is practiced on the posterior axillary line to

introduce a laparoscopic Satinsky clamp directly through the

abdominal wall (Fig. 3).

The space between the abdominal wall and kidney can be

too narrow or the renal parenchyma too thick to use a

laparoscopic clamp. No preoperative criteria can predict this

setting. In these cases, a standard Satinsky clamp (B. Braun

Aesculap, reference B504R) can be used. The jaws of the

standard Satinsky clamp are much wider, but the clamp is

shorter than the laparoscopic clamp. A wet swab can be rolled

around the clamp at the point of penetration into the

abdominal wall to reduce CO2 leakage. The CO2 insufflator

compensates the leakage of gas around the clamp. This

procedure was necessary in four patients because of the

thickness of renal parenchyma at the site of clamping. The

renal parenchyma is clamped at distance from the tumour

edge (Figs. 4 and 5). This distance is evaluated macroscopically

and after evaluation of the preoperative computed tomo-

graphy (CT) scan. No more than 30% of the whole parenchyma

is clamped during this step. A line on the capsule is marked with

the monopolar diathermy to determine the line of incision. The

lesion is excised withcold scissors toallow a betterevaluationof

the resection margins by the pathologist (Fig. 6) and sent for

frozen section analysis. In case of positive margins, wider

resection can be performed, theoretically. However, it did not

occur in this series. Minor bleeding vessels are cauterised with

standard reusable bipolar electrocautery. Bigger vessels and the

collecting duct system are repaired with a monofilament of

polyglecaprone absorbable Monocril 4/0 if necessary. Biologic

glue composed of bovine serum albumin and glutaraldehyde

(Bioglue1, Cryolife International) is then applied on the whole

dry resection bed, with the use of the laparoscopic applicator.

One application appears to be sufficient in this initial

experience. The Satinsky clamp is carefully released. The

kidney is inspected for bleeding. The perirenal fat is finally

sutured. In case of larger or deeper tumours, when glue is likely

to be insufficient, a conventional parenchymal suturing

technique can be applied provided that the clamp has been

placed enough distant from the tumour edge.

Fig. 6 – The resection of the tumour can be easily performed

in an almost bloodless field.

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All data concerning age, gender, ASA score, tumour size,

preoperative and postoperative serum creatinine levels, and

length of stay were recorded. Intraoperative data were also

noted and included operative time, need to repair the collecting

duct system, estimated blood loss, blood transfusion, margin

size, and complications. Pathologic tumour stage and grade

were determined according to the 2002 TNM version [10].

3. Results

Two men and three women underwent this proce-dure. Their mean age was 67.8 yr (range: 58–78 yr).

Table 1 – General characteristics of the population

Patient 1 Pati

Age, yr 58 68

Sex Male Fema

ASA score 2 2

Indication Elective Elect

Tumour size, cm 6 3

Tumour location Lower pole Lowe

Preoperative serum creatinine level, mg/l 11.9 14.9

Postoperative serum creatinine level, mg/l 15.1 9.2

Length of stay, days 8 6

Histology Clear cell Clear

Fuhrman grade 2 2

Table 2 – Operative outcomes

Patient 1 Patien

Operating time, min 330 180

Type of approach Transperitoneal Retroperit

Repair of the collecting duct system Yes No

Margin size, mm 1 1

Blood loss, ml 150 —

Blood transfusion No No

Mean tumour diameter was 3.06 cm (range: 1.3–6 cm). All the patients were operated for electiveindications. One lesion was located at the upper poleand four at the lower pole. General characteristics ofthe patients are shown in Table 1. The meanpreoperative serum creatinine concentration was11.5 mg/l (range: 9.9–14.9 mg/l). Mean postoperativeserum creatinine level was unchanged at 10.9 mg/l(range: 8.6–15.1 mg/l). Length of stay was 8 days onaverage (range: 6–10 d).

Mean operative time was 238 min. There wasno conversion. Mean blood loss was 250 ml (range:150–600 ml), and no blood transfusion was neces-sary. The collecting duct system was repaired in onepatient with a 6-cm lesion. No complication wasnoticed intraoperatively or postoperatively; in par-ticular there were no urine or blood collections, andno injury of the renal capsule caused by the Satinskyclamp was recorded. All the results are listed inTable 2. Resection margins were tumour free in allcases. The final pathologic examination revealedclear cell carcinoma in three patients and angio-myolipoma and oncocytoma in one patient each.

4. Discussion

Surgery remains the only curative treatment forrenal cell carcinoma. It is now clearly establishedthat nephron-sparing surgery remains the goldstandard approach in tumours <4 cm. Laparoscopic

ent 2 Patient 3 Patient 4 Patient 5

71 64 78

le Female Female Male

2 3 2

ive Elective Elective Elective

3.5 1.3 2

r pole Upper pole Lower pole Lower pole

10.6 10.4 9.9

8.6 11.9 9.8

7 9 10

cell Clear cell Angiomyolipoma Oncocytoma

3 — —

t 2 Patient 3 Patient 4 Patient 5

300 180 200

oneal Transperitoneal Retroperitoneal Transperitoneal

No No No

3 1 0

150 600 100

No No No

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partial nephrectomy has progressively emerged as asafe alternative to open surgery [3]. The 5-yroncologic and renal functional outcomes of laparo-scopic and open partial nephrectomy are compar-able [11]. The main objectives of this technique areto obtain a bloodless operative field, thereforeavoiding positive resection margins and allowingan easy closure of the pelvicaliceal system alongwith minimal morbidity and length of hospital stay.

In the first series of laparoscopic partial nephrec-tomy, procedures were performed without control-ling the renal vessels, but using different types ofhaemostatic instruments [12]. This was to avoidwarm renal ischaemia, but resulted in a moredifficult demarcation between tumour and normaltissue and was associated with higher complicationrates. Guillonneau et al compared results of laparo-scopic partial nephrectomy with and withoutclamping of the renal pedicle in 28 patients; therewas a significantly higher mean blood loss inpatients without hilar occlusion [9]. A few otherseries confirmed the decreased blood loss obtainedwith clamping of the renal pedicle, and some alsofound a lower incidence of positive margins sug-gesting that clamping the renal artery should beroutinely performed [4,13,14].

However, the harmful effects of warm ischaemiashould not be underestimated. Alternatives havebeen tested to limit these findings, such as renalhypothermia [15]. The kidney is placed in an Endo-bag, the pedicle is clamped, and ice slush is disposedall around. Mean ischaemia time was 43.5 min andno effect was observed on the serum creatininelevel. But clamping the hilum after ice insertionappears to be difficult, with the risk of inadequateocclusion and bleeding. Air leakage was also aproblem, as much as bag slippage, resulting in alimited workspace. Similarly, Janetschek et aldescribed a technique of renal artery perfusion withiced Ringer’s lactate, after percutaneous retrogradeinsertion of an angiocatheter into the main renalartery through a femoral puncture [16]. Primaryresults were encouraging by facilitating vascularrepair during surgery while no damage to renalparenchyma was noticed on postoperative isotopescans. Recently, several teams have studied theeffect of warm ischaemia on serum creatininelevels. In a study including 118 patients, Bhayaniet al. [17] found no statistical difference in pre-operative and postoperative serum creatinine levelsamong patients with warm ischaemia time<30 min.Even if mean preoperative and postoperative serumcreatinine levels seem to be higher in patients whohad an occlusion >30 min, the difference was notstatistically significant. These findings were not

affected by adjustment for age, sex, tumour size, orestimated blood loss. Gill’s team confirmed theseresults in 179 patients [18]. MAG3 renal scintigraphywas performed in 12 patients and found a calculatedreduction of function from baseline of 29%, gen-erally corresponding to the importance of theresection. Both concluded that ischaemia has lowand acceptable effects on renal function if limited to1 h. However, strong scientific evidence is stilllacking and it could also be postulated that thereduced renal function is due to ischaemic damage.It is also impossible to evaluate the impact on overallrenal function based on postoperative creatininevalues as long as the contralateral kidney isfunctional. In a study including 55 patients, Abukoraand colleagues compared the effects on renalfunction between patients operated under warmor cold ischaemia [19]. They noticed a slight increasebetween preoperative and postoperative creatininelevels in both groups, whereas there was a sig-nificant reduction in the postoperative split functionof the treated kidney. However, parenchymaldamages were noted in some patients even if theischaemic time was relatively short and even withcold ischaemia. Based on contradictory data thatexist in the literature, caution must be thereforerecommended until further studies are available.

Several teams are trying to find new techniques inanimal models to avoid clamping of the renalvessels. The main advantage would be no dissectionof the renal vessels, which can reduce operativetime, but more particularly to preserve the rest ofthe normal renal parenchyma and reduce the risk ofmicroscopic lesions and acute tubular necrosis, asobserved immediately after laparoscopic partialnephrectomy when the renal artery has beenclamped, even if it reverted with time [18]. Testsusing potassium-titanyl-phosphate laser in a por-cine model appeared to be attractive, with noperioperative complications and blood loss<30 ml. But smoke in the operative field reducedvisibility and significantly increased the meanoperating time. This led the authors to clamp thepedicle to reduce smoke formation [20]. Ong et alreported a technique in a porcine model usingbipolar needle electrocautery inserted into the renalparenchyma and applied transversely, creatinglocalised ischaemia. The lesion was then excisedwith cold scissors. However, temporary arterialcontrol for haemostasis was necessary in 17% ofcases [21]. Microwave tissue coagulation was alsotested in 19 patients, but with several postoperativecomplications: haematoma, urine leakage, renalarteriovenous fistula, and progressive kidneydestruction ending in a nonfunctional state [22].

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Another main problem mentioned by all the authorsis the renal tissue damage induced by these differentenergies, with an area between 2 and 4 mm ofcoagulative necrosis from the line incision that canhide positive margins. Moreover, a Japanese teamshowed on CT scans that 4–10% of the surgicallyspared renal tissue was not functional after micro-wave tissue coagulation [23]. Our technique offersthe advantage of reproducing the open techniqueusing a Satinsky clamp, with the benefits of thelaparoscopic approach. No one has previouslydescribed this technique during laparoscopy eventhough parenchymal clamping has already beendescribed during open partial nephrectomy [24].Bleeding can be progressively controlled, and thelimits of the resection are clearly exposed. Excisioncan be done with no hurry or fear of renal ischaemia.Nevertheless, indications are still limited to periph-eral lesions. Sometimes the laparoscopic Satinskyclamp appears too short to allow a good control andexcise the lesion safely, but it can be easily replacedby a normal Satinsky clamp for open surgery.

Suturing in laparoscopy is also difficult and timeconsuming. Different tissue sealants are commer-cially available, reducing operative times andpotentially reducing morbidity. In a hypertensiveporcine model, Johnston et al compared sevendifferent agents [25]. The experience showed thatfor small and medium resections, thrombin/gelatingranules (FloSeal1) were quite effective, allowingreaction with local residual blood clot. However,FloSeal1 appeared less effective in wider resections.BioGlue1 (not tested in Johnston’s study) seems topresent comparable results, but is cheaper thanother agents [26]. Our study confirmed thesefindings. Applied on a dry field, BioGlue1 achievedadequate haemostasis in all five patients. However,many strategies exist in laparoscopic surgery forachieving adequate haemostasis. To date, none hasdemonstrated total efficacy and safety [27].

We recognise that our technique is not exemptfrom limitations mainly because it cannot beobviously applied to all patients and tumours. Thistechnique is more likely to be applied to tumours<4 cm in size and peripherally located. Central orhilar tumours cannot be resected with this tech-nique due to the impossibility of placing the clamp.Haemostatic agents can be easily used alone insimple cases as was the situation in this initialreport but they appear to be more expensive and lessreliable than suture repair in more challengingcases. However, we believe that this technique inwell-selected cases allows tumour resection in abloodless field, collecting system repair, and evenparenchymal conventional suturing techniques

when necessary while avoiding prolonged warmischaemic times.

5. Conclusion

We present our initial experience of laparoscopicpartial nephrectomy with clamping of the renalparenchyma in five patients. This technique can beperformed in selected patients with peripherallesions. The procedure avoids warm ischaemia ofnormal parenchyma, allowing the surgeon to oper-ate in an almost bloodless field. Additional experi-ence is necessary to confirm the safety of thistechnique.

Conflicts of interest

None declared.

Appendix A. Supplementary data

Supplementary data associated with this articlecan be found, in the online version, at doi:10.1016/j.eururo.2007.04.072 and via www.europeanurology.com. Subscribers to the printed journal will find thesupplementary data attached (DVD).

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