Robot-Assisted Retroperitoneal Lymphadenectomy in Testicular Cancer Treatment: A Systematic Review

Abstract

Introduction:

Retroperitoneal lymph node dissection (RPLND) in testicular cancer is a documented treatment along with active surveillance and chemotherapy. This study aims to summarize the current evidence on the use of Robot-assisted RPLND (RARPLND) in comparison with the laparoscopic and open approach.

Materials and Methods:

A search was conducted in the existing literature focusing on reports with outcomes of RARPLND for stage I-IIB testicular tumor.

Results:

Eleven studies complied with the inclusion criteria, including 116 patients. The average follow-up of 21.2 months showed no retroperitoneal recurrence. The median lymph node yield was 22.3 and the overall positive rate was 26%. Complications were encountered in 8% of the patients. The robotic approach showed similar results to the laparoscopic approach and outperformed the open procedure in perioperative parameters.

Conclusions:

Relapse-free survival, nodal yield, and complication rates during RARPLND for clinical stage I-IIB are acceptable. Further studies are required to establish these findings and determine benefit from the use of robotic approach.

Introduction

Testicular cancer affects a considerable portion of young men and can be treated with great cure rates reaching a 5-year survival of 99% in early stage disease.¹ On a worldwide basis, the preferred therapeutic strategy after orchiectomy seems to differ slightly; active surveillance, chemotherapy, and retroperitoneal lymph node dissection (RPLND) are all well-accepted approaches. In stage IA disease active surveillance holds the lead. On the contrary, for early stage IB up to IIB of non-seminomatous germ cell tumors (NSGCT), chemotherapy and RPLND are gaining ground. In such cases, complication rates along with short- and long-term side effects of each approach determine the appropriate treatment. Along with active surveillance, the National Comprehensive Cancer Network (NCCN) directives² propose both primary RPLND and chemotherapy as appropriate for clinical stage (cstage) IB disease, in contrast with the European Association of Urology (EAU) guidelines,³ which appear to favor adjuvant chemotherapy. This is supported by the higher recurrence rates of 7% in case of primary RPLND in comparison to chemotherapy reported in a publication from German Testicular Cancer Study Group.⁴ Both Guideline committees lean toward interventional treatment options in cstage IB disease, in view of high risk of metastasis or inability to adequately adhere to surveillance schedule, while definitely recommend them in IIA and IIB stage patients. In favor of the surgical approach is the accurate staging achieved since about 30% of the patients with no findings in noninvasive staging examinations will prove to have occult retroperitoneal metastases.

Besides open approach, RPLND may also be performed implementing minimal invasive surgery principles. The open approach demands a midline or thoracolumbar incision for transperitoneal and retroperitoneal approach, respectively. On the other hand, the laparoscopic approach first proved feasible about 14 years ago and is now indicated only when adequate experience exists.⁵ Along with the improved cosmesis and convalescence, the oncologic equivalence but also a tendency to fewer complications was shown. However, the high rates of adjuvant chemotherapy in stage II disease, the high levels of expertise demanded for the procedure and the relatively low incidence led to a limited spread of the technique.⁶

The robotic era entered this field 10 years ago.⁷ This new platform brings several aids to the minimally invasive toolbox that may be able to overcome the steep learning curve and technical limitations inherent to the laparoscopic approach. Small series and case reports were reported, yet no direct unicentral comparative or prospective analysis has been made. As any new procedure, the Robot-assisted RPLND (RARPLND) must prove equivalent in terms of safety and oncological outcomes before it can be recommended as a standard of care.

The aim of this review is to summarize the current evidence on the use of Robot-assisted RLND, with emphasis on oncological outcomes and safety along with a comparison to the open and laparoscopic approach.

Materials and Methods

Search strategy and data sources

A thorough review of the literature was performed in accordance to the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines (Supplementary Table S1; Supplementary Data are available online at www.liebertpub.com/lap).⁸ Identification of eligible studies was performed using the PubMed (Medline) database through September 2017. The following MeSH terms were utilized in various combinations: “retroperitoneal lymph node dissection,” “retroperitoneal lymphadenectomy,” “robot–assisted,” “robotic,” “testicular,” “testis,” “NSGCT,” “non-seminomatous” and “nonseminoma.” Two independent reviewers (A.T., D.M.), screened all articles retrieved by the search algorithm. Reference lists of the included studies were further assessed to identify any potentially eligible studies.

Inclusion & exclusion criteria

All studies were assessed for eligibility based on the following criteria: (1) the study should report outcomes of robot-assisted retroperitoneal pelvic lymph node dissection in men due to testicular cancer; (2) contain stage I-IIB tumors; (3) the study should report outcomes regarding the number of nodes excised and/or the percentage of infiltration by tumor; (4) recurrence rates and follow-up should be reported; (5) the study should report perioperative and/or postoperative complications. Articles were excluded if they met at least one of the following criteria: (1) congress communications and abstracts; (2) reviews; and (3) studies reporting on minimally invasive retroperitoneal lymphadenectomy for other types of malignancies.

Data extraction and tabulation

Two independent reviewers (A.T., D.M.) reviewed the full-texts of eligible studies, performed the data extraction, and cross-checked all results. The following parameters were extracted from each study: study features (first author, journal, and year of publication) and surgical and pathological parameters (age, clinical stage, laterality, and postoperative chemotherapy). Also, data on lymph node yield and positivity, relapse and mean follow-up time and mean operative time (OT), estimated blood loss (EBL), length of hospital stay, complication rates, and conversion to open were extracted. Descriptive statistics were used to summarize the clinical outcomes.

Results

Search results and study characteristics

The initial search algorithm yielded 1450 records. Following screening of titles and abstracts, 33 studies were retrieved for full-text evaluation. Ten studies were deemed eligible, while 1 was identified from their reference lists for a total of 11 retrospective studies included in the analytic cohort (Fig. 1). In total, 116 patients underwent RARPLND for testicular cancer (Table 1). Eligible studies were published from 2006 onward and all were retrospective case reports and case series. From each study, only NSGCT cases staged I-IIB were included, regardless of undertaking primary or salvage RARPLND. The mean age of participants was 29 years (range, 18–67 years). The clinical stage, laterality of the procedure, and demand for adjuvant chemotherapy postoperatively are presented on Table 1. Only one study contained a comparison to laparoscopic approach.⁹

FIG. 1.

Flowchart of the search strategy.

Table 1.

Demographics of the Patients Included in the Systematic Review

								Laterality (%)
No.	Authors	Journal	Year	Mean age	No. of patients (N = 116)	cstage	Postop chemo (%)	L	R	Bi
1	Davol et al.⁷	Journal of Urology	2006	18	1	I	0	0	0	100
2	Annerstedt et al.¹¹	Journal of Robotic Surgery	2008	42	3	II PC	NR	33	66	0
3	Williams et al.²⁸	European Urology	2011	31	3	I	0	0	100	0
4	Kamel et al.¹²	Journal of Robotic Surgery	2012	21.5	2	II PC	0	50	50	0
5	Cost et al.¹⁴	Journal of Endourology	2012		2	I-II	1 (50)	0	50	50
6	Cobelli et al.³⁹	World Journal of Urology	2012	28.3	3	I	0	66	33	0
7	Dogra et al.¹⁵	Urology Annals	2013	23	1	I	0	0	100	0
8	Cheney et al.¹⁶	BJU International	2015	32.2	18	I:66%II:44%	8 (44)	NR	NR	NR
9	Harris et al.⁹	BJU International	2015	29.8	16	I	0	50	50	0
10	Stepanian etal.¹³	European Urology	2016	31.2	18	I:67%II:33%	4 (20)	35	35	30
11	Pearce et al.¹⁷	European Urology	2017	30	49	I:89%II:11%	5 (62)	53	47	0

Bi, bilateral; cstage, clinical stage; L, left; NR, not reported; PC, postchemotherapy; R, right.

Surgical approach of RPLND

In the vast majority of cases, the da Vinci robotic system was used to perform RPLND. The surgical technique differed; the lateral approach was the most prominent, followed by the superiorly sited robotic arms. Both needed undocking for bilateral cases. Overcoming the aforementioned hindrance, a new supine approach exploits the rotational capabilities of the Xi system.

In general, especially the largest series adhered to the traditional open templates.¹⁰ Left side nerve sparing templates contained the removal of the gonadal vein, left common iliac, preaortic, para-aortic, and retroaortic lymph nodes up to the inferior mesenteric artery. Some removed interaortocaval lymphatic tissue. For right-side, excision extended to the gonadal vein, right common iliac lymph nodes, paracaval, precaval, retrocaval, interaortocaval, and preaortic inferior mesenteric artery. The superior limit was the renal hilum and ureter was the lateral one. Nerve-sparing was based on the decision of the surgeon. A single center performed frozen section on the three largest lymph nodes proceeding in a bilateral excision in patients with viable germ cell tumor. Bilateral dissection contained all the lymphatic tissue between left and right ureter as lateral borders and between renal hilum and inferior mesenteric artery in addition to ipsilateral iliac nodes and gonadal vein. Administration of postoperative chemotherapy was based on the decision of each multidisciplinary oncologic team.

Oncological outcomes

All included reports included patients with disease of cstage I up to IIB. Due to lack of evidence 2 of the 11 articles were not included in this part of our review.^11,12 Thus, the remaining 9 reports containing, 111 patients, were analyzed for oncological parameters (Table 2).

Table 2.

Summary of Oncological Parameters

No.	Authors	Year	No. of patients (N = 111)	LN yield	LN positivity	Retroperitoneal relapse	Mean FU (months)
1	Davol et al.⁷	2006	1	21	1	0	5
2	Williams et al.²⁸	2011	3	25	0	0	13
3	Cost et al.¹⁴	2012	2	12	0	0	14.5
4	Cobelli et al.³⁹	2012	3	16.6	NR	NR	NR
5	Dogra et al.¹⁵	2013	1	13	0	0	6
6	Cheney et al.¹⁶	2015	18	22	8	0	22
7	Harris et al.⁹	2015	16	30	2	0	13.5
8	Stepanian et al.¹³	2016	18	19.5	7	0	49
9	Pearce et al.¹⁷	2017	49	26	8	0	16
Average				24.2	6.3 (26%)	0	21.2

FU, follow-up; LN, lymph node; NR, not reported.

The mean follow-up period was 21.1 months with 49 months being the largest mean interval.¹³ No retroperitoneal, in surgical site, relapse was revealed during this period and no diseasespecific mortality was reported. Another parameter of the quality of the dissection is the lymph node yield. In our analysis the average count was 24 lymph nodes (LNs) (interquartile range [IQR] 26–22), with the lowest number being 12–13 LNs in 2 small series.^14,15 The mean lymph node positivity rate for malignancy was 6.3 LNs that corresponds to percentage of 26% (IQR 24%–29%).

Peri- and postoperative outcomes

Table 3 summarizes the operative and postoperative outcomes of RARPLND. Mean OT was 263 minutes (IQR 293–235), and EBL was 76 mL (IQR 75–50). Only one transfusion took place administering 2 U of red blood cells but further details on this case were not provided.¹⁶ The median length of postoperative stay varied among studies from 1 to 4 days, but the mean was 1.3 days. The centers with the largest series had a postoperative hospitalization of only 24 hours.^13,17

Table 3.

Summary of Operative and Postoperative Outcomes of Robot-Assisted Retroperitoneal Lymph Node Dissection

No.	Authors	Year	N	OT (minutes)	Transfusion	EBL (mL)	Clavien I-II	Clavien III-IV	Ejaculation antegrade (%)	Conversion
1	Davol et al.⁷	2006	1	235	0	125	0	0	100	0
2	Annerstedt et al.¹¹	2008	3	143	0	43	NR	NR	NR	0
3	Williams et al.²⁸	2011	3	187	0	166	0	0	100	0
4	Kamel et al.¹²	2012	2	207	0	450	0	0	NR	0
5	Cost et al.¹⁴	2012	2	442	0	53	0	0	100	0
6	Cobelli et al.³⁹	2012	3	243	0	50	0	0	100	0
7	Dogra et al.¹⁵	2013	1	210	0	450	0	NR	100	0
8	Cheney et al.¹⁶	2015	18	329	1	103	2	0	91	3
9	Harris et al.⁹	2015	16	271	NR	75	0	1	100	1
10	Stepanian et al.¹³	2016	18	293	0	50	0	1	90	0
11	Pearce et al.¹⁷	2017	49	235	0	50	2	2.1	97	1
Average				263	0.01	76	4	4	95.5	5.5

N = 116.

EBL, estimated blood loss; NR, not reported; OT, operative time.

Complications

Complication rates were reported in 8% of the patients. Most frequently, postoperative complications were reported using the Clavien-Dindo classification of surgical complications.¹⁸ Minor complications were encountered in 4% of the patients, whereas major complications were observed in an equal 4%. Ileus and chylous ascites were reported in minute percentages. Conversion rates were up to 5.5% due to robot malfunction, poor surgical field, and blood loss that could not be contained in a robotic laparoscopy setting. The debilitating complication of retrograde ejaculation was found in 4.5% of the cases.

Discussion

The surgical excision and biopsy of the testicle is followed by three management options in men with early-stage NSGCTs; active surveillance, a course of chemotherapy and RPLND. The factors for decision making are the possibility of relapse, level of toxicity for each patient, and adherence to the demanding schedule of active surveillance protocols.

In favor of surveillance is the fact that 2/3 of the patients with stage I NSGCT can be cured by orchiectomy alone. Salvage chemotherapy is an excellent option if relapse is documented by vigorous follow-up. On the other hand accumulative radiation exposure due to CT scans should be considered.

Chemotherapy is readily offered in many hospital settings with excellent results but cannot eliminate retroperitoneal teratoma and long-term follow-up is still required. Chemotherapeutic drug's side effects and the hazard of cardiovascular disease and secondary neoplasms cannot be easily overridden.¹⁹

The surgical approach in cstage I is based on the fact that retroperitoneal lymph nodes are the first metastatic site. In this population, occult metastases will be diagnosed in 15% to 25% with chemoresistant retroperitoneal teratoma. Moreover, especially in case of bilateral lympadenectomy, relapse in surgical site is scarce allowing for wider intervals of follow-ups. The rates for cT1 and teratoma are high and adjuvant chemotherapy can be avoided in 75%, with no retroperitoneal metastases. Furthermore, antegrade ejaculation rates are excellent in case of nerve sparing templates.

According to EAU guidelines, RPLND has lost ground after a publication of the German Testicular Cancer Study group compared it to chemotherapy. Administration of one scheme of BEP (bleomycin, etoposide, and cisplatin) as adjuvant treatment revealed a more than 7% recurrence rate difference.²⁰ Between 18 to 30% of patients have concomitant metastases in the retroperitoneal lymph nodes (pStage II). RPLND is the most capable means of detecting these lesions and therefore offering accurate staging, nevertheless, the surgical approach has not overcome the curative potential of chemotherapy. Moreover, about 10% of pStage I finally metastasize in distant sites. In presence of metastases and no chemotherapy administration, recurrence will be found in 31% of the patients.³

Thus, the indications for RPLND are based on the histology report classification and the clinical stage. In case of cstage I and an NSGCT type all three of the aforementioned treatment options offer cure. It is a fact that the 30% of patients with concurrent metastases, that are not detectable with the noninvasive staging techniques, will lose the opportunity of cure if surveillance is chosen.²¹ Lymphovascular invasion and embryonal carcinoma on initial histological examinations are signs of metastatic potential and surveillance only is not proposed in this group.^3,22 In cstage IIA and IIB the controversy concerns the sequence of surgery and chemotherapy. Either RPLND and adjuvant chemotherapy or chemotherapy and postchemotherapy (PC) RPLND offer excellent prognosis of 95%.²³ PC-RPLND is advised in remaining masses after chemotherapy in stages IIC and III and in some cases of seminomas.²¹

It is the perioperative morbidity that is open RPLND surgical approach's main disadvantage. Furthermore, the relative rarity of the incidence of the disease and the special demands in surgical technique renders the surgical approach not so easily available. This is why multicenter studies revealed more complication rates and recurrences than specialized centers.³ The introduction of minimally invasive approaches as the laparoscopic-PLND and RARPLND surgery offer a more compelling choice.

During the 65 years of practice, open procedure was evolved in nerve sparing RPLND with standardized lymph node templates to avoid the debilitating complication of retrograde ejaculation in young male patients. In 1992 pioneers Hulbert and Fraley²⁴ as well as Rukstalis and Chodak⁵ were the first to implement the laparoscopic approach. Such procedure was soon proved to be possible in PC surgical field, which is in general more demanding.²⁵ Later on, when the experience spread and the procedure evolved, case series showed faster convalescence, less blood loss, and less complications.^9,26 The opposition claimed the need for laparoscopic expertise and the ability to handle vascular complications, fewer lymph node yield, inadequate dissection near the great vessels, and administering of adjuvant chemotherapy in too many cases of pN1 staging.^9,27 The controversy ended and the efficacy of the procedure has been well established as far as oncological outcomes are concerned. However, these approaches are not widespread and are approved for use in specialized centers.³

A new push to the minimally invasive approach promised to ameliorate the ailments of the laparoscopic approach. The well-known advancements of robotic surgery brought the ability of 3D visualization and the extreme accuracy and stability in confined spaces were readily implemented in minimally invasive RPLND as well.

First and foremost, equivalence to the former approaches is to be shown. Davol et al. reported for the first time in 2006⁷ a full-bilateral lymph node dissection with promising perioperative postoperative and oncological results. They performed a bilateral RPLND showcasing that excision of lymphatics posterior to the great vessels reaching the lumbar veins was possible. Length of stay (LOS) was only 2 days and no complications were encountered. The patient remained disease free after 5 months with a normal ejaculation function. This primary sign could lead to a more broad use of surgical approach, in contrast with the former belief of laparoscopy execution mainly for staging.²¹

More case and small series reports came to light pointing to the same direction, both in stages I-II and in PC settings. Williams et al. published a 3-case series reporting left Robotic RPLND implementing a nerve-sparing template. The patients were discharged after 2 days with no complications. Mean LN yield was 25 (12 to 33). One year follow-up showed excellent functional outcome and no relapse.²⁸ Additionally, Cost et al. in a 2-case report had similar outcomes and were the first to execute the robotic approach in a PC setting for stage II testicular cancer. Next followed Dudderidge et al. showing a series in PC patients with comparable results.²⁹ Cheney et al. analyzed a series of 18 patients, 8 of them in a PC setting. There were 3 cases of conversion to open due to hemorrhage, difficult surgical field, and robot malfunction. The outcomes fluctuated in a similar manner to the previous cases, and in accordance to our analysis. The follow-up showed no recurrence (mean 22 months) at the retroperitoneal site, but revealed 2 cases of pulmonary lesions. Ejaculatory function was maintained normal in 91% of the patients. The authors stated that there were no major perioperative differences in primary and PC procedures except for better OT favoring the former. In addition, they reported the feasibility of clearing out all the retroperitoneal disease and no patients were administered adjuvant chemotherapy.^16,21

The first and only one to date comparative retrospective study, between 16 RARPLND and 21 L-RPLND cases was reported by Harris et al.⁹ in 2015. The series of 1 surgeon were analyzed and revealed no difference in OT, EBL, lymph node dissection, and ejaculatory function. Thus, possible superiority of the robotic approach was yet to be proved.

The largest single surgeon series to our knowledge is from Stepanian et al. presenting an OT of 293 minutes, blood loss of 50 mL, and 1 day of hospital stay. In this study, a small case series was operated with the novel da Vinci Xi robotic system. The capabilities of the platform allow for retroperitoneal and spermatic cord dissection without the need for undocking, thus hinting to a lower OT.¹³

A USA multicenter study featuring the largest number of a total of 49 patients showed excellent results. The OT was 235 minutes, blood loss was impressively low at 50 mL, mean nodal yield was 26, and LOS was only 1 day in all cases. There were two intraoperative complications, one of which was vascular, due to the unclamping of an aortal branch that led to open conversion. The 2-year survival rate was 97%.^9,17

Some advocate that a vascular injury during robotic RPLND will be devastating due to the distance of the surgeon and the undocking time needed before the conversion to open. Proposed safety measures are the readiness of the appropriate instruments and an extra trocar aiding surgical field view and allow for bleeding control while laparotomy is executed.¹⁷ Also, use of the Xi system offers improved reach for the assistant.¹³ A parameter not to be neglected is the financial issues. Since the novelty of the robotic technology comes to a cost, it is the significantly lower hospitalization postoperatively and complication rates that may balance the scale.³⁰

The perioperative data of our study were compared to open and laparoscopic RPLND. In general it is perioperative parameters where robotic approach outperforms traditional practice. According to our review the RARPLND average operating time was 263 minutes, higher but comparable to the open series (186/188/270 minutes). The hospitalization postoperatively was kept at a low of 1.3 days in comparison with 3.3/4.1/6.6 days after the open approach. Moreover, blood loss was eliminated from 184/450 mL in open series to 76 mL. The largest and more specialized centers of this review showed even stronger difference with 1 day LOS and 50 mL EBL.^6,30–32 In comparison with L-RPLND the results are more or less on par as in laparoscopic procedures. EBL was reported as 50, 125, and 184 mL, OT was 185/204/291 minutes and LOS of 2 to 3.3 days. The overall complication rate in our study was 8% which is considered acceptable since open series show percentages of 7%–24%.^6,9,33,34 No pulmonary and surgical trauma infections were documented, in contrast with the respective 2% and 5% in the open approach.^17,35

Approaching the oncological equivalence issue, we try to compare indicative data. The lymph node yield was found to be 24.2 that is close but slightly less than the open series' 28–38 LNs and greater than L-RPLND's 16 LNs, though only stage I cases were included in the latter.^6,36,37 The infiltrated nodes were found to be as expected at 26%, similar to the open series (19%–30%) and 25% for the laparoscopic ones. As far as the recurrence-free survival is concerned, the absence of retroperitoneal relapse in a mean follow-up time of 21.2 months is reassuring but the interval is rather short to conclude safely on this issue. However, in view of the fact that the recurrences in cstage I occur in the first 24 months at a 95% rate, it is indeed a promising finding.^17,38

Several methodological biases of the studies included in the present analysis exist and are well worth reporting. First of all, all the data presented herein come from retrospective studies, whose value is limited compared to their prospective counterparts. Furthermore, not all of the studies use standardized tools of reporting and multiple surgeons with varying levels of experience and training were executing those procedures. We contained data from the first developmental stages of the robotic approach that may not be now representative. The inclusion of both cstage I and II, as well as some limited PC cases in the same study cannot reveal more specific data and solid comparisons for either of them as contamination errors will be apparent. Thus, the percentage of positive lymph nodes will be lower in cstage I only cases. The length of follow-up showed inconsistency throughout the reports and may be another potential bias in terms of complication rates, as the intraoperative and immediate postoperative period includes events up to 3 months after surgery. Finally, most of the data analyzed herein come from high-volume centers and thus the reproducibility of the results presented may be difficult among less experienced surgeons.

Conclusion

RARPLND appears to have an acceptable safety profile when compared to open surgery that is currently considered as the gold standard approach. In addition, antegrade ejaculation was in acceptable percentage in experienced surgical centers. Preliminary results of the curative potential of this novel minimally invasive procedure are encouraging, although larger cohort studies with adequate follow-up are needed to validate these results and determine a possible benefit over open and laparoscopic approach.

Authors' Contributions

Study conception and design: A.T., D.M., A.P; acquisition of data: A.T., D.I.T., A.P; analysis and interpretation of data: E.F., E.M., P.S., M.V., A.P; drafting of article: A.T., D.M., D.I.T; critical revision: A.P., D.I.T., D.M.

Footnotes

Disclosure Statement

No competing financial interests exist.

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