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obot-assisted Pelvicymphadenectomy for Bladderancer—Where Have We Reached By 2009

qbal Singh

BJECTIVES To review the current status and role of robot-assisted laparoscopic pelvic lymphadenectomy. Toreview the need, extent, lymph node yield, oncological feasibility, and outcome of robot-assistedpelvic lymphadenectomy for invasive bladder cancer in patients undergoing a robot-assistedlaparoscopic radical cystectomy.

ETHODS The National Library of Medicine and the Pub Med were extensively searched for the cases ofrobot-assisted laparoscopic pelvic lymphadenectomy performed in conjunction with robot-assisted laparoscopic radical cystectomy for bladder cancer using the following keywords: bladdercancer, pelvic lymphadenectomy, cystectomy, laparoscopy, robot, and robot-assisted radicalcystectomy. These were reviewed and analyzed (using certain tabulated parameters) to determinethe current status of robot-assisted pelvic lymphadenectomy.

ESULTS The search yielded about 12 major published series (278 cases) of “robot-assisted radicalcystectomy with pelvic lymphadenectomy,” with an overall acceptable mean operating time(s),complication rate, blood loss, and hospital stay.

ONCLUSIONS Robot-assisted laparoscopic pelvic lymphadenectomy in conjunction with robot-assisted laparo-scopic radical cystectomy is an oncologically feasible and technically safe procedure withacceptable early operative outcomes that appear to be comparable to those achieved with

open/laparoscopic surgery. UROLOGY 75: 1269–1274, 2010. © 2010 Elsevier Inc.

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he pelvic lymph nodes (LNs) are the most com-mon sites for metastasis from bladder cancer andare seen in up to one-fourth of the patients un-

ergoing radical cystectomy (RC) for invasive bladderancer. The frequency of this is known to increase withhe increase in the tumor stage. Despite aggressive mul-imodal management, up to three-fourths of patients withnown pathologic nodal involvement may develop recur-ences. Currently, pelvic lymphadenectomy (PLND)erves as one of the important prognostic markers forrothelial bladder cancers. Limited debate exists on theole of PLND for patients undergoing cystectomy fornvasive bladder cancer, although the extent of LN dis-ection and oncological feasibility of robot-assistedLND is still not clearly defined. We have reviewed andiscussed the status and role of robot-assisted laparo-copic PLND for management of invasive bladder urothe-ial cancer.

rom the Department of Urology, Wake Forest University Medical School and Baptistedical Center, Medical Centre Boulevard, Winston Salem, North CarolinaReprint requests: Iqbal Singh, M.D., M.Ch.(Urology), Department of Surgery

Urology), University College of Medical Sciences (University of Delhi) and GTBH,-14 South Extension Part-2, New Delhi-110049, India. E-mail: iqbalsinghp@

bahoo.co.uk

Submitted: August 3, 2009, accepted (with revisions): November 6, 2009

2010 Elsevier Inc.ll Rights Reserved

HY IS THERE A NEEDOR LYMPHADENECTOMYN BLADDER CANCER?ccording to the anatomical and lymphatic mapping

tudies, the primary regions of lymphatic drainage of therinary bladder (UB) are perivesical, hypogastric, obtu-ator, external iliac, and presacral nodes. The lymphaticsrom prostate, trigone, and posterior bladder wall drainnto the presacral nodes. The regional LNs draining the

B lie in the true pelvis below the bifurcation of theommon iliac artery. The secondary landing sites arehe common iliac, inguinal, and para-aortic/caval LNsjuxtaregional nodes). Pelvic nodal metastasis tends to oc-ur in approximately 25% of patients undergoing RC.1,2

The most common sites of metastases in bladder can-er are the pelvic LNs; among these, obturator nodes arenvolved in approximately 74%, external iliac nodes in5%, paravesical nodes in 16%, presacral nodes in 25%,nd juxtaregional common iliac LNs in 20% of patients.3

he overall incidence of LN positivity in bladder canceraries from 10% to 40% depending upon the stage ofisease.4 Despite current multimodal management, about0% of patients with pathologic nodes are known toevelop recurrence(s).5 PLND thus provides the vitalaseline data with respect to disease staging, therapeutic

enefit, and prognostic information.

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HAT ARE THE TYPES OF PELVICYMPHADENECTOMY THAT ARE FEASIBLEND WHAT SHOULD BE THE EXTENTF PELVIC LYMPHADENECTOMY �TANDARD OR EXTENDED?n ideal PLND must be able to clear the entire LN

rainage basin of the UB. It must also maintain thenatomical boundaries of dissection, demanding a highegree of meticulousness of the surgeon and/or the robot,nd be able to provide a specimen yield that is consis-ently able to maintain a high LN density.

Four types of PLND have been described in the publishedata: (i) Limited PLND, which includes removal of LNs ofainly the obturator region; (ii) Standard PLND, includes

emoval of all LNs from the bifurcation of common iliacessels proximally, from the genitofemoral nerves laterally,ith the tissue around deep circumflex iliac vein, Cloquetodes, and femoral canals till the hypogastric vessels distallynd obturator fossa posteriorly; (iii) Extended PLND, whichn addition includes a standard PLND with a cephaladxtension to the level of aortic bifurcation, including theresacral nodes; (iv) Super-extended PLND, which is aore extensive PLND that extends more proximally up to

he level of inferior mesenteric artery.6

There is another term “modified PLND,” mentioned inhe published data, it was first described by Weingartnert al in 19967 in relation to pelvic LN dissection inadical prostatectomy. Many authors8-10 have used theerm since then synonymously with “standard PLND”nd describe it as a LN dissection technique, whichncludes obturator and hypogastric LNs up to the bifur-ation of common iliac artery. However, the term “mod-fied PLND” has been used more frequently in conjunc-ion with radical prostatectomy for prostate cancer. Forhe sake of uniformity we shall avoid using the termmodified PLND” in this manuscript throughout the text.

The answer to the question what ought to be thextent of PLND in bladder cancer is based on the resultsf LN mapping studies.11-13 These suggest that obturatorodes (74%) are the most common site of metastaticisease,11 and in case these were involved, the commonliac nodes are the next most commonly involved inbout 19%,12,13 thus strongly supporting a case for rou-ine extended PLND. Some studies have also indicated aossible therapeutic benefit of systematic bilateral PLND,hereby implicating extrapelvic disease as a major deter-inant of patient survival.11 These mapping studies also

upport the fact that when metastatic disease was locatedn the pelvic and common iliac nodes, the nodes abovehe aortic bifurcation were involved in about another0% of cases.3 According to Abol-Enein et al,14 extend-ng the surgical template of PLND from limited to stan-ard and from standard to extended resulted in raisinghe probability of complete clearance of the disease from3% to 65% and from 65% to 79%, respectively, therebyndicating that extended PLND still fails to achieve

omplete clearance in about 20% of the patients. Simi- d

270

arly, others12 have also reported that involvement of theodes above the aortic bifurcation was observed in 35%f cases whenever the common iliac nodes were in-olved, thereby implying that skip lesions were rarelyncountered. According to Abol-Enien et al,14 skipodal metastasis are rarely seen and the endopelvic re-ion (comprising the obturator and internal iliac nodes)erves as the sentinel area, with negative endopelvicodes thus indicating that proximal dissection may note necessary. This supports the case against superex-ended PLND on a routine basis. However, in caseshere the primary bladder tumor arose from the posteriorall and/or the trigone, the presacral nodes were in-olved in up to 9% of cases.14 This has led others todvocate superextended PLND, particularly in patientsith high-grade invasive bladder cancer.15 Even though

ecent evidence seems to suggest improved outcomes, theoutine use of extended PLND in bladder cancer stillemains debatable.14,16,17 However, according to Bruinst al,15 the therapeutic benefits (in terms of staging andurvival) of extended bilateral PLND exist both in nodeositive as well as node-negative bladder cancer after RC.oods et al17 have also reported on the precision, safety,

easibility, and reproducibility of robot-assisted PLND, aseing one of the chief advantages and benefits of thispproach. According to the “Will Rogers phenomenon,”outine use of a PLND among patients harboring minimalodal disease serves to enrich node (�) patients (remov-

ng tumor burden) and the same in node (�) patientsremoving undetectable micrometastases) will minimize pa-ients with node(�) disease, thus enhancing patient sur-ival in both groups, thereby suggesting a therapeutic ben-fit.15 According to Dhar et al,18 after RC, a limited PLNDs associated with suboptimal staging, inferior outcome foratients with node (�) and node (�) disease, and a higherate of local progression. Thus, extended PLND allows forore precise staging and enhanced survival of patients withode (�) disease. The potential therapeutic benefits ofLND are also briefly described in Table 1.In our opinion, standard bilateral PLND is fundamentally

ecessary. There is also growing body of evidence to suggesthat extended PLND in patients with invasive bladder can-er (undergoing RC) including nodes up to the aortic bi-urcation and the presacral nodes is likely to be associatedith significantly improved oncological outcomes.3,12,13,31,32

HAT FACTORS AFFECT THE SEVERALNS EVALUATED IN A PLND SPECIMEN?ome workers1,33,34 have relied on the concept of LNensity (tumor burden [ratio of the positive nodes]: ex-ent of dissection [total LN yield]). The concept of LNensity was probably first described by Stein et al in003,35 as a means to define, prognosticate, and stratifyatients with nodal metastatic bladder cancer. After aeview of at least 10 major published studies on LNensity by Stein et al,2 the most commonly reported LN

ensity cut off for predicting decreased disease-specific

UROLOGY 75 (6), 2010

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urvival after RC in bladder cancer was about 20%. Innother review by Kassouf et al and others,36 the prog-ostic importance of LN density was further highlightedy their conclusion that it was superior to tumor lymph-ode metastasis nodal stage in predicting disease-specificurvival after RC irrespective of the adjuvant chemother-

Table 1. Review of cases of robotically-assisted radical cy

Authors Content Complication

Gamboa et al.,19

200941 RALRC (�) Margin,

2 (4.9%)

Pruthi et al.,20

200950 RALRC 40(M) �

10(F)(�) Margin, 0

Comp rt � 1 (2%)

Guru et al.,21

200867 RALRC �

RPLND(�) Margin,

6 (8.9%)1-vascular injury

Pruthi et al.,22

200820 RALRC (�) Margin, 0

Comp rt �6 (30%)

Murphy et al.,23

200823 RARC (�) Margin, 0

Comp rt �6 (26%)

Wang et al.,24

200833 RALRC vs 21

open RC(�) Margin, 2 (6%(�) Margin, 3Comp rt, 9.9%

Abraham et al.,25

200714 RALRC vs 20

LRC(�) Margin, 1 (7%

Comp rt, 4 (28%)21% RALRC50% LRC

Guru et al.,26

200720 RALRC (�) Margin,

3 (15%)Comp rt, 2 (10%)

Rhee et al.,27

20067 RALRC vs 23

open RC(�) Margins, 0

Comp � Nil

Hemal.,28

200421(M) � 3(F) (�) Margins, 0

Menon et al.,29

20043RALRC (F) �

IC/ONB(�) Margins, 0

Menon et al.,30

200314 (M) � 3(F)

RALRC � IC(�) Margins, 0

Total cases 278 RALRC Average comp rttime � 10%

RALRC indicates robotic-assisted laparoscopic radical cystectomy;ORT � operating room time; EBL � Estimated blood loss; ECUDpositive surgical margins; Comp rt � complication rate.* Figures depicted in Table 1 are computed from published manu

py status. Thus, the numbers of positive nodes as well as a

ROLOGY 75 (6), 2010

he total number of nodes dissected (extent of dissection)re extremely important prognostic factors. The onlyther statistically significant predictor of survival afterC for bladder cancer is the presence of LN invasion

extracapsular extension).37 Other additional importantrognostic factors are the pathologic stage of the tumor

tomy and PLND*

Outcome Conclusion

an no. LNs excised-25 (4-68)an ORT/EBL � 8.29/254 mLan HS � 8 (5-37)

Operative outcomescomparable to openRC

an no. LNs excised �9 (12-34)

Oncological goals met inall patients.

an ORT/EBL � 4.6 h/215 mLan HS � 4.9 dan no. LNs excised � 18 Oncologically acceptable

extend PLNDan ORT(RPLND) � 44 minan no. LNs excised �9 (6-29)

Oncologically acceptableshort-term outcomes.ECUD

an ORT/EBL � 6.1/313 mLan HS � 4.3 dan no. LNs excised �6 (8-25)

Acceptable early oncol.outcome. ECUD

an ORT/EBL � 6.6 h/278 mLan of HS � 11.6 d. f LNs excised � 20 vs 17 Similar LN yieldjor complications, 3 vs 4 PSM Rt � not significant

ECUD. of LNs excised � NS-22 vs6

Oncologicallyacceptable. ECUD

T/EBL � NS (6.6 h)/212 (vs653)

. LNs excised � 13 (6-26) Oncologically safe

an EBL, 555 mL.T � 3.3 h (RARC), 45 min(PLND)an HS, 10dan ORT/EBL � 8.4 vs 10.6/1109 vs 479 mL

Significantly lower

an HS � 11 vs 13 d Min blood lossECUD

. LNs excised � 3-27 Acceptable outcomean ORT/EBL � 3.8-5.8/100-300 mL

Min blood loss/morbidity

an HS � 4-5 d ECUDan no. LNs excised � 12 Acceptable outcomean ORT/EBL � 2.66 h/100

mLan HS � 6.6 d

Preservation of uterus/vagina ECUD

. LNs excised � 4-27 Acceptable outcomean ORT/EBL � 2.3/�150 mL

Nerve-sparing technique.Conversation 1

erage blood loss/ORT �64/6.82

Feasible

D � Robotic pelvic lymphadenectomy; RC � Radical cystectomy;tracorporeal urinary diversion; M � males; F � females; PSM �

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HAT IS THE CURRENTTATUS OF ROBOTIC PLND AND ISROBOTIC EXTENDED PLND FEASIBLE?

n the report published by Menon et al,30 their 17 casesf robot-assisted laparoscopic RC with PLND set thetage open for robot-assisted RC and PLND. The tech-ique of robot-assisted laparoscopic PLND was, however,ecently published and described by Woods et al in008.17 According to Stein et al38 an extended PLND isurrently recommended as a necessary component of RCor treating invasive bladder cancer.

Although Herr et al (2004)39 proposed standards forC and PLND in a major systematic review of over 1000f multi-institutional cases cystectomy for all stages ofladder cancer that the mean acceptable number of LNsxcised should be at least 15 (with an extended PLNDeing required approximately 75% of times, with tumorargins � 10%); nevertheless Woods et al (2008)17

tated in their study that there is no established minimumumber of nodes that ought to be removed at the time ofC. An exhaustive review of published manuscripts on

obot-assisted laparoscopic PLND with robotic cystec-omy summarized by us in Table 1 clearly shows that theumber of LNs harvested with robotic PLND does notppear to be lower compared with the open standard of0-14.17 Other experienced robotic urologists,20-28,38-40

ave also shown that this is not only acceptable, feasible,nd adequate with regard to the LN count, but is alsoonsidered oncologically safe as in experienced hands itarely adds another 30-45 minutes to the operating roomime of RC without significantly compromising patientorbidity in any way.21,22,26 Guru et al21 also recently

emonstrated in their last 11 patients that a properxtended PLND (robot assisted) was feasible retrieving aean of 23 LNs, with a mean operating time of 44inutes. The use of the 4-arm robot may facilitate an

xtended PLND. Going by the criteria of LN density too,right et al 34 have clearly demonstrated in their cohort

f 1260 patients (patients of RC with PLND, no distantetastasis and at least 1 positive LN) that the incremen-

al benefit to survival in LN-positive cancer was likelyestricted to 10-14 nodes only, thereby suggesting thathe total number of nodes resected by robotic extendedLND (Table 1) were oncologically adequate.Robot-assisted laparoscopic PLND is an oncologically

easible procedure that can be safely performed in womenoo, with the advantage of preserving the uterus andagina29 or it can be combined with an anterior pelvicxenteration.20 It also appears to be an oncologicallyiable, acceptable, and efficient procedure with regard tohe LN count and density, when it comes to reviewinghe current intermediate term follow-up. According to

oods et al17 and Gamboa et al19 too, an extendedobotic PLND is oncologically feasible and viable butay require certain modifications in the technique such

s a more cranial placement of the robotic ports and using

he fourth arm of the newer S-version of the DSRS p

272

Da-Vinci surgical robotic system) to aid in retraction ofhe sigmoid colon. Reports suggest that an extendedLND may be associated with improved clinical out-omes.16 Another advantage of robotic extended PLNDs the ease of submitting the LN specimens as separateackets (up to 13); proponents of submitting separateackets include Ather et al,41 Boucher et al,42 and Steint al,43 who have reported the association of a higher LNield when PLND specimens are submitted as separateackets compared with an en bloc submission. Accordingo Lerner et al,44 techniques such as robotic-assistedaparoscopic cystectomy must maintain the surgical stan-ard of anatomic PLND and provide reliable long-termancer control equivalent to that achieved by open RCnd bilateral pelvic and iliac node dissection. In a recenttudy by Pruthi and Wallen,45 in 50 patients who under-ent robot-assisted standard (28 patients) and extended

22 patients) PLND the authors concluded that the ef-cacy of robot-assisted laparoscopic PLND was compara-le to open surgical approaches for managing bladderancer.

ONCLUSIONs robotic PLND an oncologically feasible procedure?efinitely yes, as the resected LN count appears to beore than adequate. This is clearly supported by several

eported cases in the published English data as shown inable 1. Is robotic PLND an oncologically efficaciousrocedure with regard to bladder cancer? Yes, based onhe current perioperative short-term and intermediateollow-up. Should robot-assisted PLND be an extendedr standard PLND? This appears to be still debatable,ven though recent evidence seems to be in favor of anxtended PLND. Should the specimen be submitted aseparate packets vs en bloc resection? Separate packets doppear to be associated with a better LN yield. Whathould be the minimum standard with regards to numberf LNs to be excised in PLND for bladder cancer? Noxed numbers exists, but as a general standard this maye perhaps, 15-18. Timing of PLND, should it be beforer after RC? Preferably, PLND may be easier after a RC,ecause of more space being available to better accom-odate the robotic instruments within the tight confines

f the bony pelvis. What are its long-term results? Al-hough the early and intermediate overall operative out-omes appear to be favorable, the long-term results areot known, as the data regarding long-term follow-up ofobot-assisted laparoscopic RC is still awaited.

Thus, with experience, robot-assisted laparoscopic PLNDs now considered oncologically feasible and acceptableoth in the men as well as in women with invasive bladderancer. The use of the robot allows a more meticulousissection17 in areas around the inferior mesenteric arteryaortic bifurcation proximally); hence, it is oncologicallyfficient for harvesting all the PLNDs with regard to the LNensity and number of LNs harvested. With regard to early

erioperative outcomes, intermediate oncological efficacy

UROLOGY 75 (6), 2010

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surgical margins and LN yield) robot-assisted laparoscopicC appears to favorably compare with laparoscopic RC andpen RC; however, long-term outcomes are still awaited.n the basis of current reports in the published data, about

78 robot-assisted laparoscopic radical cystectomies haveeen performed worldwide from 12 centers (comprisingbout only 4% of total number of cystectomies performedorldwide for bladder cancer). Until long-term objectiveata on oncological control and functional data becomevailable, the precise role of robot assistance in RC andLND remains to be evaluated. Nevertheless, robot-assisted

aparoscopic radical cystectomy has the potential to expandn the near future.

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UROLOGY 75 (6), 2010