Secondary Logo

Journal Logo

Comparative effectiveness of minimally invasive versus open lymphadenectomy in urological cancers

Prasad, Sandip M.a; Shalhav, Arieh L.b

doi: 10.1097/MOU.0b013e32835af286
ROBOTICS: Edited by Jim Hu
Free

Purpose of review With increasing adoption of minimally invasive surgical techniques in urologic oncology, the efficacy, safety, and adequacy of lymphadenectomy were reviewed for studies about prostate, bladder, kidney, upper tract urothelial, testicular, and penile cancer published in the past 18 months.

Recent findings In prostate cancer, in which robotic prostatectomy has become the predominant approach, use of extended lymphadenectomy has increased with lymph node yield nearing 20. Minimally invasive lymphadenectomy in bladder cancer does not yet approach the yield seen at high-volume open cystectomy centers, but a larger proportion of robotic lymph node dissections surpass the oncologic threshold of 10–14 lymph nodes compared with open surgery. Comparative lymphadenectomy data for kidney and upper tract urothelial cancers remain muddled as routine lymphadenectomy is not performed and both open and laparoscopic/robotic nephroureterectomy carry no consensus on templates. Minimally invasive retroperitoneal lymph node dissection carries safety and oncologic equivalence to the open technique only in limited centers, whereas minimally invasive ilioinguinal lymphadenectomy for penile cancer remains exploratory at this time.

Summary Findings from the prior year suggest that – in high-volume centers – lymph node dissection for urologic cancers is equivalent between open and minimally invasive techniques in lymph node yield and short-term to medium-term oncologic results.

aDepartment of Urology, Medical University of South Carolina, Charleston, South Carolina

bSection of Urology, University of Chicago Hospitals, Chicago, Illinois, USA

Correspondence to Sandip M. Prasad, MD, MPhil, MUSC Department of Urology, 96 Jonathan Lucas Street, Clinical Science Building 644, Charleston, SC 29425, USA. Tel: +1 843 792 5783; fax: +1 843 792 8523; e-mail: prasads@musc.edu

Back to Top | Article Outline

INTRODUCTION

Although perioperative benefits of minimally invasive surgery are well documented in urologic oncology, uncertainty over quality and oncologic outcomes of laparoscopic and robotic lymphadenectomy compared with the gold standard open approach remains a critical issue. Although minimally invasive approaches to lymph node dissection (LND) technically duplicate the open technique, comparative effectiveness studies are needed to ensure the safety and adequacy of the procedure as the quality of LND influences survival [1]. Eradication of tumor within lymph nodes may reduce or eliminate the risk of regional recurrence. Additionally, greater sampling of lymph nodes may improve staging and early detection of metastatic disease to proffer more timely adjuvant therapy. Finally, the completeness of a LND may represent overall surgical quality.

In the absence of well designed and appropriately powered randomized phase III trials to compare open versus minimally invasive lymphadenectomy, existing literature is primarily composed of retrospective and prospective studies as well as population-based databases. We will review data regarding the comparative effectiveness of minimally invasive (laparoscopic or robotic) and open lymphadenectomy for prostate, bladder, kidney, upper tract urothelial, testicular, and penile cancers. A systematic review was performed in July 2012, searching MEDLINE articles from the previous 18 months using a combination of search terms listed in Appendix 1. We excluded unpublished data and non-English language articles.

Box 1

Box 1

Back to Top | Article Outline

Prostate cancer

The first laparoscopic lymphadenectomy for staging of prostate cancer was performed in 1991 [2]. Subsequently, the role of routine pelvic lymphadenectomy in prostate cancer management has been debated as stage migration in the prostate-specific antigen screening era has decreased the likelihood of positive lymph nodes at radical prostatectomy [3–5]. The decrease in concomitant lymphadenectomy at radical prostatectomy has also been attributed to the adoption of minimally invasive surgical techniques over the same period [6]. A population-based study reported that in Medicare beneficiaries who underwent radical prostatectomy, pelvic LND (PLND) was performed in 83% of open cases compared with 17% of laparoscopic and robotic surgeries [7]. After controlling for D’Amico risk group as well as demographic and clinical variables, this relationship persisted [odds ratio of performing PLND during open versus minimally invasive radical prostatectomy: 16.7; 95% confidence interval (CI), 11.1–25.0] [8▪▪].

There is a paucity of well designed, multiinstitutional randomized clinical trials comparing open and minimally invasive radical prostatectomy [9–11]. Although initial studies suggested that minimally invasive PLND might be inferior to the open procedure [12], improvements in lymph node yield positivity rate, PLND complication rate, and operative time are recognized as part of the learning curve in robotic radical prostatectomy [13▪]. More contemporary studies from high-volume centers (including our own [14]) have established that laparoscopic and robotic PLND have comparable lymph node yield (median: 13–21 lymph node), complication rates, and oncologic outcomes to open lymphadenectomy in both standard and extended surgical templates [15,16]. We performed an extended PLND (ePLND; Fig. 1[17▪]) in all men with prostate cancer, with the exception of those with National Comprehensive Cancer Network (NCCN) defined [18] very low-risk prostate cancer as the existing NCCN nomogram may significantly underestimate the rate of lymph node invasion in those men with a predicted risk of 2% or less [19,20]; a significant proportion of positive lymph nodes in high-risk men will be outside the obturator fossa [21,22]; and ePLND improves cancer-specific survival (CSS) in men with intermediate-risk and high-risk prostate cancer independent of nodal status [23▪]. For minimally invasive ePLND, rates of symptomatic lymphoceles or intraoperative complications are less than 1–5% in high-volume centers [24–26].

FIGURE 1

FIGURE 1

Within the past 18 months, the majority of publications report technical modifications or serve as confirmatory studies to the efficacy of lymphadenectomy; selected studies are discussed herein. In a comparative series of over 800 radical prostatectomies with standard PLND, mean lymph node yields were greater during robotic versus open radical prostatectomy (7.1 versus 6.0, P < 0.001) in cohorts matched for demographic and clinical characteristics [27▪▪]. Davis et al. [28] reported an increase in lymph node yield from a median of 5–16 lymph nodes after adopting extended versus standard PLND. Yuh et al. [29] demonstrated that robotic ePLND to the common iliac bifurcation can be performed safely and with excellent lymph node yield (median 20 lymph nodes, interquartile range 15–25). In cases wherein intraperitoneal surgery may be contraindicated (e.g., extensive prior abdominal surgery), the extraperitoneal approach did not compromise the oncologic efficacy or safety of minimally invasive LND in a study of over 550 patients. [30▪]. Finally, the role of technology does not appear to have modified LND yield as Shah and Abaza [31] studied the effect of lymph node yield performed on two generations of robotic surgical platforms (the first-generation robot and the daVinci S) and noted no difference (10.7 versus 10.6 lymph nodes).

Back to Top | Article Outline

Bladder cancer

Thorough lymphadenectomy for bladder cancer was championed by Skinner [32] as it may influence survival with metastasis present up to 30% of the time at surgery [33]. A single small randomized trial [34] and the majority of retrospective and prospective matched case–control studies have reported no difference in lymph node yield between open, laparoscopic, and/or robotic cystectomy [35–37], although some groups have reported higher nodal yield with the robotic approach [38▪]. Comparative analysis of oncologic outcomes between open and minimally invasive cystectomy is confounded by selection bias as the majority of minimally invasive series had a small proportion of patients with nonorgan-confined disease and nodal metastases [39,40]. Although there is no debate regarding the value and importance of LND at radical cystectomy, the surgical approach and anatomic extent of dissection remain controversial. At present, two actively recruiting multi-institutional randomized clinical trials comparing open and robotic cystectomy (National Cancer Institute sponsored R01 study) and standard LND versus eLND (Southwest Oncology Group 1011 trial) may provide answers regarding the comparative effectiveness of the various approaches.

Multiple studies in the past 18 months have demonstrated that laparoscopic and robotic LND can achieve satisfactory lymph node yield (standard of care of 10 nodes or more (which only 40% of open cystectomy cases in population-based studies satisfy [41] compared with 83% of robotic surgeries in a multi-institutional study of 527 cystectomies [42▪,43]). Two other multi-institutional cohorts with more than 650 combined patients undergoing robotic LND both reported a mean number of 18 lymph nodes removed at cystectomy [44,45]. Treiyer et al. [46] reported robotic LND with mean lymph nodes above this benchmark, with Desai et al. [47] reporting a median yield of 42 lymph nodes with minimally invasive extended LND to the level of the inferior mesenteric artery. In a small case–control series of eLND, the mean lymph node yield was no different in the open (36.9 ± 14.8) and robotic (37.5 ± 13.2) groups with a similar positive node rate (30 versus 34%) [17▪]. As the minimally invasive cystectomy experience grows, there does not appear to be diminished efficacy of LND in high-risk patients. Lymph node yield was statistically similar between open and robotic cystectomy in the elderly (≥ 70 years of age) [48▪,49].

Back to Top | Article Outline

Kidney cancer

The role of lymphadenectomy in the surgical management of primary renal cell cancer remains controversial. A phase 3 randomized clinical study comparing radical nephrectomy to radical nephrectomy with lymphadenectomy demonstrated no survival advantage to a regional LND in conjunction with extirpative surgery [50]; however, this study was limited by inclusion of primarily low-risk patients, lack of statistical power to demonstrate equivalence between treatment arms, and nonstandardized surgical templates without reporting of lymph node yield [51]. Only 6.6% of over 37 000 patients who underwent radical nephrectomy from the SEER database from 1988 to 2005 received a LND [52▪]; in a more contemporary period, concurrent lymphadenectomy occurred in only 11% of cases [53]. LND is not routinely performed in the absence of gross lymphadenopathy, given the low rate of positive nodes without radiographic or visual suspicion [54]. If LND is performed, an extended template dissection (Fig. 2[55]) is indicated as increased lymph node yield is associated with improved CSS in patients with lymph node-positive nonmetastatic renal cell carcinoma [56▪▪].

FIGURE 2

FIGURE 2

Comparative studies between open and minimally invasive partial or radical nephrectomy during the study period did not report systematic LND or excluded those cases in which lymphadenectomy was performed [57,58]. Abaza and Lowe reported the initial series of robotic LND for renal cell carcinoma (RCC) in 36 patients with a mean of 14 lymph nodes [59▪▪]; the authors noted an increase from 11 to 17 lymph nodes in the second half of cases, exceeding the benchmark of 12 lymph nodes needed to maximize detection of nodal metastases [60]. This is the first study reporting lymph node yield during minimally invasive oncologic renal surgery to exceed the benchmark, as no prior study exceeded a mean of eight lymph nodes [61–64]. Comparative long-term oncologic data are lacking given the lack of routine lymphadenectomy following nephrectomy in most series.

Back to Top | Article Outline

Testicular cancer

Adoption of laparoscopic retroperitoneal lymph node dissection (RPLND) has been utilized in clinical stage I nonseminomatous germ cell tumors since 1992 [65], with robotic RPLND first reported in 2006 [66]. Concerns regarding the completeness of dissection, potential tumor dissemination from pneumoperitoneum, and technical difficulty with dissection posterior to the great vessels has limited adoption of minimally invasive RPLND to limited centers. Oncologic efficacy of minimally invasive RPLND has been questioned due to heterogeneity of surgical technique (sampling versus curative intent), variability of templates, and high rates of chemotherapy in patients with pN1 disease compared with open RPLND [67].

Initial studies of laparoscopic RPLND reported lower lymph node yield than open surgery, concerning for inferior therapeutic value [68,69]. Within the past 18 months, studies from centers performing minimally invasive RPLND with therapeutic intent (rather than for biopsy or staging) report node counts and intermediate-term recurrence rates replicating open surgical results [67,70–73]. Hyams et al. [67] report that 91 patients who underwent laparoscopic RPLND had intraoperative complication rates less than 5% and postoperative complication rates less than 10%. Mean lymph node count was 26 with 31% of patients having retroperitoneal metastases. Follow-up at a mean of 38 months demonstrated no evidence of relapse. Gardner et al. [70] demonstrated similar perioperative complication rates in 59 patients who underwent laparoscopic RPLND, including 13 with prior chemotherapy. Mean lymph node count was 22 with a single retroperitoneal recurrence. There are no published studies of tumor dissemination by pneumoperitoneum, and port site and local metastasis may occur without the use of specimen bags and careful tissue handling (especially of more fragile cystic lesions) is more likely the culprit in reported cases of port site metastases and remains paramount during specimen manipulation and extraction [74,75].

Back to Top | Article Outline

Upper tract urothelial cancer

Similar to renal tumors, the role of lymphadenectomy for upper tract urothelial carcinoma (UTUC) remains controversial. Although advocates of LND note the common histologic origin with bladder cancer and data supporting the survival benefit in cystectomy patients [76], UTUC has a distinct cause, anatomy, and lymphatic drainage patterns that argue against automatic extrapolation [77]. Half of patients with UTUC globally [78] and 74% of patients in the USA [79] undergo LND. eLND at nephroureterectomy may be curative in patients with low-volume nodal disease [80▪▪], but this conclusion merits further validation.

The majority of previously published studies suggest than LND is less common in patients undergoing minimally invasive compared with open nephroureterectomy [although with similar lymph node counts (median = 8 nodes) and CSS] [81–83], but these are small series with variable dissection templates [84,85]. A single randomized trial has been performed comparing laparoscopic and open nephroureterectomy, but LND was not performed [86]. In the past year, published studies have minimally elucidated the relationship between the two surgical approaches. Ni et al. [87] published a systematic review including over 4300 patients undergoing nephroureterectomy comparing the efficacy and safety of laparoscopic and open nephroureterectomy and found that LND was only performed in 10 of 21 studies, limiting the authors’ ability to draw conclusions. A systematic review and meta-analysis of nephroureterectomy by Rai et al. [88] included 20 studies but did not discuss lymphadenectomy. Both Ariane et al. [89] (609 patients) and Walton et al. [90] (773 patients) compared open and laparoscopic nephroureterectomy, but regional LND was performed only when nodal involvement was suspected preoperatively or discovered intraoperatively. A population-based analysis examining over 8000 patients who underwent either open or laparoscopic nephroureterectomy did not contain data regarding LND [91]. Only one study reported nephroureterectomy yield; Abe et al. [92▪] performed a case–control series of 80 patients wherein regional LND was performed in both open and laparoscopic cases and demonstrated a median of 10 lymph nodes removed in both groups.

Back to Top | Article Outline

Penile cancer

Despite its attractiveness given the morbidity of open lymphadenectomy, the use of minimally invasive inguinal lymphadenopathy has only been described in a small number of patients [93–96]. In the past 18 months, two new centers adopted and presented their results for laparoscopic and robotic inguinal LND. Britto et al. [97] reported laparoscopic bilateral inguinal lymphadenectomy yielding 31 lymph nodes without perioperative complications, whereas Dogra et al. [98] reported robotic bilateral inguinal LND (Fig. 3[98]) in two patients discharged home in 48 h without complication. Although minimally invasive ilioinguinal LND has no long-term data, its potential to reduce the morbidity of the open technique remains promising.

FIGURE 3

FIGURE 3

Back to Top | Article Outline

CONCLUSION

The practice and extent of LND in urological cancers remain controversial, independent of the use of minimally invasive techniques. Robotic LND in prostate cancer has become the accepted standard and is equivalent or superior to the open technique. For bladder cancer, selection bias imperils any comparison of surgical approach, and we await the results of two randomized multicenter trials. The selective use and variable templates of lymphadenectomy in kidney cancer and upper tract urothelial cancers limit comparability of the two techniques, and existing data are inconclusive regarding safety and yield. Use of minimally invasive RPLND in testicular cancer may reduce morbidity, but equivalent oncologic results are only reproducible at expert centers. In penile cancer, minimally invasive LND remains in its infancy.

Back to Top | Article Outline

Acknowledgements

None.

Back to Top | Article Outline

Conflicts of interest

There are no conflicts of interest.

Back to Top | Article Outline

REFERENCES AND RECOMMENDED READING

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • ▪ of special interest
  • ▪▪ of outstanding interest

Additional references related to this topic can also be found in the Current World Literature section in this issue (pp. 100–101).

Back to Top | Article Outline

REFERENCES

1. Herr HW. Surgical factors in bladder cancer: more (nodes) + more (pathology) = less (mortality). BJU Int 2003; 92:187–188.
2. Schuessler WW, Vancaillie TG, Reich H, Griffith DP. Transperitoneal endosurgical lymphadenectomy in patients with localized prostate cancer. J Urol 1991; 145:988–991.
3. Lu-Yao GL, Albertsen PC, Moore DF, et al. Outcomes of localized prostate cancer following conservative management. JAMA 2009; 302:1202–1209.
4. Ung JO, Richie JP, Chen MH, et al. Evolution of the presentation and pathologic and biochemical outcomes after radical prostatectomy for patients with clinically localized prostate cancer diagnosed during the PSA era. Urology 2002; 60:458–463.
5. Briganti A, Blute ML, Eastham JH, et al. Pelvic lymph node dissection in prostate cancer. Eur Urol 2009; 55:1251–1265.
6. Feifer AH, Elkin EB, Lowrance WT, et al. Temporal trends and predictors of pelvic lymph node dissection in open or minimally invasive radical prostatectomy. Cancer 2011; 117:3933–3942.
7. Prasad SM, Keating NL, Wang Q, et al. Variations in surgeon volume and use of pelvic lymph node dissection with open and minimally invasive radical prostatectomy. Urology 2008; 72:647–652.discussion 52–53.
8▪▪. Hu JC, Prasad SM, Gu X, et al. Determinants of performing radical prostatectomy pelvic lymph node dissection and the number of lymph nodes removed in elderly men. Urology 2011; 77:402–406.

Population-based report demonstrating effect of surgical approach on likelihood of PLND.

9. Guazzoni G, Cestari A, Naspro R, et al. Intra- and peri-operative outcomes comparing radical retropubic and laparoscopic radical prostatectomy: results from a prospective, randomised, single-surgeon study. Eur Urol 2006; 50:98–104.
10. Asimakopoulos AD, Pereira Fraga CT, Annino F, et al. Randomized comparison between laparoscopic and robot-assisted nerve-sparing radical prostatectomy. J Sex Med 2011; 8:1503–1512.
11. Kang DC, Hardee MJ, Fesperman SF, et al. Low quality of evidence for robot-assisted laparoscopic prostatectomy: results of a systematic review of the published literature. Eur Urol 2010; 57:930–937.
12. Guazzoni G, Montorsi F, Bergamaschi F, et al. Open surgical revision of laparoscopic pelvic lymphadenectomy for staging of prostate cancer: the impact of laparoscopic learning curve. J Urol 1994; 151:930–933.
13▪. van der Poel HG, De Blok W, Tillier C, Van Muilekom E. Robot assisted laparoscopic prostatectomy (RALP): nodal dissection results during the first 440 cases in 2 surgeons. J Endourol 2012. [Epub ahead of print]

Study demonstrating learning curve effects on lymphadenectomy during robotic surgery.

14. Zorn KC, Katz MH, Bernstein A, et al. Pelvic lymphadenectomy during robot-assisted radical prostatectomy: Assessing nodal yield, perioperative outcomes, and complications. Urology 2009; 74:296–302.
15. Eden CG, Arora A, Rouse P. Extended vs standard pelvic lymphadenectomy during laparoscopic radical prostatectomy for intermediate- and high-risk prostate cancer. BJU Int 2010; 106:537–542.
16. Wyler SF, Sulser T, Seifert HH, et al. Laparoscopic extended pelvic lymph node dissection for high-risk prostate cancer. Urology 2006; 68:883–887.
17▪. Abaza R, Dangle PP, Gong MC, et al. Quality of lymphadenectomy is equivalent with robotic and open cystectomy using an extended template. J Urol 2012; 187:1200–1204.

Case–control series demonstrating equivalence of open and robotic lymphadenectomy yield and positive node rate.

18. Mohler J, Bahnson RR, Boston B, et al. NCCN clinical practice guidelines in oncology: prostate cancer. J Natl Compr Canc Netw 2010; 8:162–200.
19. Abdollah F, Sun M, Suardi N, et al. National comprehensive cancer network practice guidelines 2011: need for more accurate recommendations for pelvic lymph node dissection in prostate cancer. J Urol 2012; 188:423–428.
20. Jayram G, Decastro GJ, Large MC, et al. Robotic radical prostatectomy in patients with high-risk disease: a review of short-term outcomes from a high-volume center. J Endourol 2011; 25:455–457.
21. Bader P, Burkhard FC, Markwalder R, Studer UE. Is a limited lymph node dissection an adequate staging procedure for prostate cancer? J Urol 2002; 168:514–518.discussion 8.
22. Joniau S, Van den Bergh L, Lerut E, et al. Mapping of pelvic lymph node metastases in prostate cancer. Eur Urol 2012. [Epub ahead of print]
23▪. Withrow DR, DeGroot JM, Siemens DR, Groome PA. Therapeutic value of lymph node dissection at radical prostatectomy: a population-based case-cohort study. BJU Int 2011; 108:209–216.

Study demonstrating that increased node yield may improve cancer-specific survival even in node-negative patients.

24. Eden CG, Zacharakis E, Dundee PE, Hutton AC. Incidence of lymphoceles after robot-assisted pelvic lymph node dissection. BJU Int 2012; 109:E14.
25. Novara G, Ficarra V, Rosen RC, et al. Systematic review and meta-analysis of perioperative outcomes and complications after robot-assisted radical prostatectomy. Eur Urol 2012; 62:431–452.
26. Clark T, Parekh DJ, Cookson MS, et al. Randomized prospective evaluation of extended versus limited lymph node dissection in patients with clinically localized prostate cancer. J Urol 2003; 169:145–147.discussion 7-8.
27▪▪. Lallas CD, Pe ML, Thumar AB, et al. Comparison of lymph node yield in robot-assisted laparoscopic prostatectomy with that in open radical retropubic prostatectomy. BJU Int 2011; 107:1136–1140.

Comparative single-institution study demonstatraing improve lymph node yield with robotic versus open PLND.

28. Davis JW, Shah JB, Achim M. Robot-assisted extended pelvic lymph node dissection (PLND) at the time of radical prostatectomy (RP): a video-based illustration of technique, results, and unmet patient selection needs. BJU Int 2011; 108:993–998.
29. Yuh BE, Ruel NH, Mejia R, et al. Robotic extended pelvic lymphadenectomy for intermediate- and high-risk prostate cancer. Eur Urol 2012; 61:1004–1010.
30▪. Mullins JK, Hyndman ME, Mettee LZ, Pavlovich CP. Comparison of extraperitoneal and transperitoneal pelvic lymph node dissection during minimally invasive radical prostatectomy. J Endourol 2011; 25:1883–1887.

Extraperitoneal lymphadenectomy is equivalent to intraperitoneal procedure in terms of nodal yield and complications.

31. Shah K, Abaza R. Comparison of intraoperative outcomes using the new and old generation da Vinci(R) robot for robot-assisted laparoscopic prostatectomy. BJU Int 2011; 108:1642–1645.
32. Skinner DG. Management of invasive bladder cancer: a meticulous pelvic node dissection can make a difference. J Urol 1982; 128:34–36.
33. Kassouf W, Leibovici D, Munsell MF, et al. Evaluation of the relevance of lymph node density in a contemporary series of patients undergoing radical cystectomy. J Urol 2006; 176:53–57.discussion 7.
34. Nix J, Smith A, Kurpad R, et al. Prospective randomized controlled trial of robotic versus open radical cystectomy for bladder cancer: perioperative and pathologic results. Eur Urol 2010; 57:196–201.
35. Styn NR, Montgomery JS, Wood DP, et al. Matched comparison of robotic-assisted and open radical cystectomy. Urology 2012; 79:1303–1308.
36. Khan MS, Challacombe B, Elhage O, et al. A dual-centre, cohort comparison of open, laparoscopic and robotic-assisted radical cystectomy. Int J Clin Pract 2012; 66:656–662.
37. Richards KA, Hemal AK, Kader AK, Pettus JA. Robot assisted laparoscopic pelvic lymphadenectomy at the time of radical cystectomy rivals that of open surgery: single institution report. Urology 2010; 76:1400–1404.
38▪. Gondo T, Yoshioka K, Nakagami Y, et al. Robotic versus open radical cystectomy: prospective comparison of perioperative and pathologic outcomes in Japan. Jpn J Clin Oncol 2012; 42:625–631.

Study demonstrating superior nodal yield with robotic versus open cystectomy/lymphadenectomy.

39. Cha EK, Wiklund NP, Scherr DS. Recent advances in robot-assisted radical cystectomy. Curr Opin Urol 2011; 21:65–70.
40. Chade DC, Laudone VP, Bochner BH, Parra RO. Oncological outcomes after radical cystectomy for bladder cancer: open versus minimally invasive approaches. J Urol 2010; 183:862–869.
41. Wright JL, Lin DW, Porter MP. The association between extent of lymphadenectomy and survival among patients with lymph node metastases undergoing radical cystectomy. Cancer 2008; 112:2401–2408.
42▪. Hellenthal NJ, Hussain A, Andrews PE, et al. Lymphadenectomy at the time of robot-assisted radical cystectomy: results from the International Robotic Cystectomy Consortium. BJU Int 2011; 107:642–646.

Multi-institutional study regarding lymphadenectomy for bladder cancer during cystectomy.

43. Hollenbeck BK, Ye Z, Wong SL, et al. Hospital lymph node counts and survival after radical cystectomy. Cancer 2008; 112:806–812.
44. Hellenthal NJ, Hussain A, Andrews PE, et al. Lymphadenectomy at the time of robot-assisted radical cystectomy: results from the International Robotic Cystectomy Consortium. BJU Int 2011; 107:642–646.
45. Smith AB, Raynor M, Amling CL, et al. Multiinstitutional analysis of robotic radical cystectomy for bladder cancer: perioperative outcomes and complications in 227 patients. J Laparoendosc Adv Surg Tech A 2012; 22:17–21.
46. Treiyer A, Saar M, Butow Z, et al. Robotic-assisted laparoscopic radical cystectomy: Surgical and oncological outcomes. Int Braz J Urol 2012; 38:324–329.
47. Desai MM, Berger AK, Brandina RR, et al. Robotic and laparoscopic high extended pelvic lymph node dissection during radical cystectomy: technique and outcomes. Eur Urol 2012; 61:350–355.
48▪. Richards KA, Kader AK, Otto R, et al. Is Robot-assisted radical cystectomy justified in the elderly? a comparison of robotic versus open radical cystectomy for bladder cancer in elderly ≥75 years old. J Endourol 2012; 26:1301–1306.

Comparison of lymph node yield in elderly patients.

49. Guillotreau J, Miocinovic R, Game X, et al. Outcomes of laparoscopic and robotic radical cystectomy in the elderly patients. Urology 2012; 79:585–590.
50. Blom JH, van Poppel H, Marechal JM, et al. Radical nephrectomy with and without lymph-node dissection: final results of European Organization for Research and Treatment of Cancer (EORTC) randomized phase 3 trial 30881. Eur Urol 2009; 55:28–34.
51. Studer UE, Birkhauser FD. Lymphadenectomy combined with radical nephrectomy: to do or not to do? Eur Urol 2009; 55:35–37.
52▪. Kates M, Lavery HJ, Brajtbord J, et al. Decreasing rates of lymph node dissection during radical nephrectomy for renal cell carcinoma. Ann Surg Oncol 2012; 19:2693–2699.

Only a small proportion of nephrectomy cases will also undergo lymph node dissection.

53. Filson CP, Miller DC, Colt JS, et al. Surgical approach and the use of lymphadenectomy and adrenalectomy among patients undergoing radical nephrectomy for renal cell carcinoma. Urol Oncol 2011.
54. Jamal JE, Jarrett TW. The current role of lymph node dissection in the management of renal cell carcinoma. Int J Surg Oncol 2011; 2011:816926.
55. Capitanio U, Becker F, Blute ML, et al. Lymph node dissection in renal cell carcinoma. Eur Urol 2011; 60:1212–1220.
56▪▪. Whitson JM, Harris CR, Reese AC, Meng MV. Lymphadenectomy improves survival of patients with renal cell carcinoma and nodal metastases. J Urol 2011; 185:1615–1620.

Performing an extended lymph node dissection improves cancer-specific survival in patients with lymph node-positive nonmetastatic RCC.

57. Jeon SH, Kwon TG, Rha KH, et al. Comparison of laparoscopic versus open radical nephrectomy for large renal tumors: a retrospective analysis of multicenter results. BJU Int 2011; 107:817–821.
58. Jeong W, Rha KH, Kim HH, et al. Comparison of laparoscopic radical nephrectomy and open radical nephrectomy for pathologic stage T1 and T2 renal cell carcinoma with clear cell histologic features: a multiinstitutional study. Urology 2011; 77:819–824.
59▪▪. Abaza R, Lowe G. Feasibility and adequacy of robot-assisted lymphadenectomy for renal-cell carcinoma. J Endourol 2011; 25:1155–1159.

First minimally invasive study in renal literature for demonstrating average lymph node more than 10.

60. Terrone C, Guercio S, De Luca S, et al. The number of lymph nodes examined and staging accuracy in renal cell carcinoma. BJU Int 2003; 91:37–40.
61. Busby JE, Brown GA, Matin SF. Comparing lymphadenectomy during radical nephroureterectomy: open versus laparoscopic. Urology 2008; 71:413–416.
62. Chapman TN, Sharma S, Zhang S, et al. Laparoscopic lymph node dissection in clinically node-negative patients undergoing laparoscopic nephrectomy for renal carcinoma. Urology 2008; 71:287–291.
63. Simmons MN, Kaouk J, Gill IS, Fergany A. Laparoscopic radical nephrectomy with hilar lymph node dissection in patients with advanced renal cell carcinoma. Urology 2007; 70:43–46.
64. Rosoff JS, Raman JD, Sosa RE, Del Pizzo JJ. Laparoscopic radical nephrectomy for renal masses 7 centimeters or larger. JSLS 2009; 13:148–153.
65. Rukstalis DB, Chodak GW. Laparoscopic retroperitoneal lymph node dissection in a patient with stage 1 testicular carcinoma. J Urol 1992; 148:1907–1909.discussion 9–10.
66. Davol P, Sumfest J, Rukstalis D. Robotic-assisted laparoscopic retroperitoneal lymph node dissection. Urology 2006; 67:199.
67. Hyams ES, Pierorazio P, Proteek O, et al. Laparoscopic retroperitoneal lymph node dissection for clinical stage I nonseminomatous germ cell tumor: a large single institution experience. J Urol 2012; 187:487–492.
68. Abdel-Aziz KF, Anderson JK, Svatek R, et al. Laparoscopic and open retroperitoneal lymph-node dissection for clinical stage I nonseminomatous germ-cell testis tumors. J Endourol 2006; 20:627–631.
69. Rassweiler JJ, Scheitlin W, Heidenreich A, et al. Laparoscopic retroperitoneal lymph node dissection: does it still have a role in the management of clinical stage I nonseminomatous testis cancer? A European perspective. Eur Urol 2008; 54:1004–1015.
70. Gardner MW, Roytman TM, Chen C, et al. Laparoscopic retroperitoneal lymph node dissection for low-stage cancer: a Washington University update. J Endourol 2011; 25:1753–1757.
71. Underwood W, Kim HL. Intermediate-term oncological efficacy of laparoscopic retroperitoneal lymph node dissection for nonseminomatous germ cell testicular cancer. BJU Int 2012; 109:281–285.
72. Ziaee SA, Tabibi A, Sharifiaghdas F, et al. Laparoscopic retroperitoneal lymph node dissection for stage I nonseminomatous germ cell testis tumors: the first case series in Iran. Urol J 2011; 8:27–30.
73. Williams SB, Lau CS, Josephson DY. Initial series of robot-assisted laparoscopic retroperitoneal lymph node dissection for clinical stage I nonseminomatous germ cell testicular cancer. Eur Urol 2011; 60:1299–1302.
74. Spermon JR, Witjes JA. Case report: the danger of postchemotherapy laparoscopic retroperitoneal lymph node dissection for nonseminomatous testicular carcinoma. J Endourol 2008; 22:1013–1016.
75. Schwartz MJ, Kavoussi LR. Controversial technology: the Chunnel and the laparoscopic retroperitoneal lymph node dissection (RPLND). BJU Int 2010; 106:950–959.
76. Herr HW, Bochner BH, Dalbagni G, et al. Impact of the number of lymph nodes retrieved on outcome in patients with muscle invasive bladder cancer. J Urol 2002; 167:1295–1298.
77. Weight CJ, Gettman MT. The emerging role of lymphadenectomy in upper tract urothelial carcinoma. Urol Clin North Am 2011; 38:429–437.vi.
78. Roscigno M, Shariat SF, Margulis V, et al. Impact of lymph node dissection on cancer specific survival in patients with upper tract urothelial carcinoma treated with radical nephroureterectomy. J Urol 2009; 181:2482–2489.
79. Lughezzani G, Jeldres C, Isbarn H, et al. A critical appraisal of the value of lymph node dissection at nephroureterectomy for upper tract urothelial carcinoma. Urology 2010; 75:118–124.
80▪▪. Roscigno M, Brausi M, Heidenreich A, et al. Lymphadenectomy at the time of nephroureterectomy for upper tract urothelial cancer. Eur Urol 2011; 60:776–783.

Lymphadenectomy in patients with low-volume nodal disease in upper tract urothelial cancer may be curative.

81. Roscigno M, Shariat SF, Margulis V, et al. The extent of lymphadenectomy seems to be associated with better survival in patients with nonmetastatic upper-tract urothelial carcinoma: how many lymph nodes should be removed? Eur Urol 2009; 56:512–518.
82. Favaretto RL, Shariat SF, Chade DC, et al. Comparison between laparoscopic and open radical nephroureterectomy in a contemporary group of patients: are recurrence and disease-specific survival associated with surgical technique? Eur Urol 2010; 58:645–651.
83. Capitanio U, Shariat SF, Isbarn H, et al. Comparison of oncologic outcomes for open and laparoscopic nephroureterectomy: a multiinstitutional analysis of 1249 cases. Eur Urol 2009; 56:1–9.
84. Abe T, Shinohara N, Muranaka M, et al. Role of lymph node dissection in the treatment of urothelial carcinoma of the upper urinary tract: multiinstitutional relapse analysis and immunohistochemical re-evaluation of negative lymph nodes. Eur J Surg Oncol 2010; 36:1085–1091.
85. Ristau BT, Tomaszewski JJ, Ost MC. Upper tract urothelial carcinoma: current treatment and outcomes. Urology 2012; 79:749–756.
86. Simone G, Papalia R, Guaglianone S, et al. Laparoscopic versus open nephroureterectomy: perioperative and oncologic outcomes from a randomised prospective study. Eur Urol 2009; 56:520–526.
87. Ni S, Tao W, Chen Q, et al. Laparoscopic versus open nephroureterectomy for the treatment of upper urinary tract urothelial carcinoma: a systematic review and cumulative analysis of comparative studies. Eur Urol 2012; 61:1142–1153.
88. Rai BP, Shelley M, Coles B, et al. Surgical management for upper urinary tract transitional cell carcinoma (UUT-TCC): a systematic review. BJU Int 2012. [Epub ahead of print]
89. Ariane MM, Colin P, Ouzzane A, et al. Assessment of oncologic control obtained after open versus laparoscopic nephroureterectomy for upper urinary tract urothelial carcinomas (UUT-UCs): results from a large French multicenter collaborative study. Ann Surg Oncol 2012; 19:301–308.
90. Walton TJ, Novara G, Matsumoto K, et al. Oncological outcomes after laparoscopic and open radical nephroureterectomy: results from an international cohort. BJU Int 2011; 108:406–412.
91. Hanna N, Sun M, Trinh QD, et al. Propensity-score-matched comparison of perioperative outcomes between open and laparoscopic nephroureterectomy: a national series. Eur Urol 2012; 61:715–721.
92▪. Abe T, Harabayashi T, Shinohara N, et al. Outcome of regional lymph node dissection in conjunction with laparoscopic nephroureterectomy for urothelial carcinoma of the upper urinary tract. J Endourol 2011; 25:803–807.

Comparison of regional lymph node dissection between open and laparoscopic nephroureterectomy.

93. Tobias-Machado M, Tavares A, Silva MN, et al. Can video endoscopic inguinal lymphadenectomy achieve a lower morbidity than open lymph node dissection in penile cancer patients? J Endourol 2008; 22:1687–1691.
94. Sotelo R, Sanchez-Salas R, Carmona O, et al. Endoscopic lymphadenectomy for penile carcinoma. J Endourol 2007; 21:364–367.discussion 7.
95. Tobias-Machado M, Tavares A, Ornellas AA, et al. Video endoscopic inguinal lymphadenectomy: a new minimally invasive procedure for radical management of inguinal nodes in patients with penile squamous cell carcinoma. J Urol 2007; 177:953–957.discussion 8.
96. Josephson DY, Jacobsohn KM, Link BA, Wilson TG. Robotic-assisted endoscopic inguinal lymphadenectomy. Urology 2009; 73:167–170.discussion 70–71.
97. Britto CA, Reboucas RB, Lopes TR, et al. Video-assisted left inguinal lymphadenectomy for penile cancer. Int Braz J Urol 2012; 38:289discussion 90.
98. Dogra PN, Saini AK, Singh P. Robotic-assisted inguinal lymph node dissection: A preliminary report. Indian J Urol 2011; 27:424–427.
Keywords:

comparative effectiveness; lymph node dissection; lymphadenectomy; urologic oncology

© 2013 Lippincott Williams & Wilkins, Inc.