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 . 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 We excluded unpublished data and non-English language articles.
The first laparoscopic lymphadenectomy for staging of prostate cancer was performed in 1991 . 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 . 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 . 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 , 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 ) 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  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].
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.  reported an increase in lymph node yield from a median of 5–16 lymph nodes after adopting extended versus standard PLND. Yuh et al.  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  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).
Thorough lymphadenectomy for bladder cancer was championed by Skinner  as it may influence survival with metastasis present up to 30% of the time at surgery . A single small randomized trial  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  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.  reported robotic LND with mean lymph nodes above this benchmark, with Desai et al.  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].
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 ; 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 . 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 . LND is not routinely performed in the absence of gross lymphadenopathy, given the low rate of positive nodes without radiographic or visual suspicion . If LND is performed, an extended template dissection (Fig. 2) is indicated as increased lymph node yield is associated with improved CSS in patients with lymph node-positive nonmetastatic renal cell carcinoma [56▪▪].
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 . 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.
Adoption of laparoscopic retroperitoneal lymph node dissection (RPLND) has been utilized in clinical stage I nonseminomatous germ cell tumors since 1992 , with robotic RPLND first reported in 2006 . 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 .
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.  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.  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].
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 , UTUC has a distinct cause, anatomy, and lymphatic drainage patterns that argue against automatic extrapolation . Half of patients with UTUC globally  and 74% of patients in the USA  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 . In the past year, published studies have minimally elucidated the relationship between the two surgical approaches. Ni et al.  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.  included 20 studies but did not discuss lymphadenectomy. Both Ariane et al.  (609 patients) and Walton et al.  (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 . 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.
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.  reported laparoscopic bilateral inguinal lymphadenectomy yielding 31 lymph nodes without perioperative complications, whereas Dogra et al.  reported robotic bilateral inguinal LND (Fig. 3) 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.
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.
Conflicts of interest
There are no conflicts of interest.
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).
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