european urology supplements 8 (2009) 470–477 available at www.sciencedirect.com journal homepage: www.europeanurology.com Consequences of Missed Nodes during Retroperitoneal Lymph Node Dissection and How to Avoid Them Giorgio Pizzocaro *, Andrea Guarneri University of Milan, S. Giuseppe Hospital, Urologic Clinic 2nd, Milan, Italy Article info Abstract Keywords: Retroperitoneal lymph node dissection (RPLND) Missed nodes Templates Prospective nerve sparing Context: Today, the role of urologic surgery in the management of nonseminomatous germ cell tumours (NSGCT) of the testis is limited to orchiectomy and post-chemotherapy surgery for residual disease. Retroperitoneal lymph node dissection (RPLND) in low stage disease is considered an optional staging procedure and templates have been introduced to avoid the risk of postoperative loss of antegrade ejaculation. Furthermore, patients with positive nodes are given adjuvant chemotherapy. Objective: To determine how best to develop templates that help surgeons to avoid missed nodes at RPLND maintaining antegrade ejaculation. Evidence acquisition: Only through a thorough understanding of the lymphatic drainage of the testis can we hope to avoid missed nodes during RPLND. This paper looks at the history of research in this area of functional anatomy as well as at the current work on the management of RPLN metastases in nonseminomatous germ cell tumours (NSGCT). Evidence synthesis: Templates that have been constructed to guide open or laparoscopic RPLND are fit for nerve sparing but are not able to avoid occasional missed nodes at RPLND. Critical evaluation of current templates suggests to extent RPLND templates to further zones. The consequence is that more extended templates can compromise antegrade ejaculation, which can be secured by prospective nerve sparing technique. Furthermore, RPLND alone will cure 70% of pathological stage IIA patients. Conclusions: Landing zones for retroperitoneal lymph node metastases are too scattered to design a restricted template that will allow both radical RPLND and an easy nerve-sparing technique to maintain antegrade ejaculation. We also have to bear in mind that chemotherapy is not a panacea for missed or recurrent nodal metastases: radical surgery does have curative potential and prospective nerve-sparing is safer than templates. # 2009 European Association of Urology. Published by Elsevier B.V. All rights reserved. * Corresponding author. Tel. +39 02 70105700/+39 335 6167380; Fax: +39 02 93660296. E-mail address: [email protected] (G. Pizzocaro). 1569-9056/$ – see front matter # 2009 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.eursup.2009.01.008 european urology supplements 8 (2009) 470–477 1. 471 Introduction Theoretically, there are several consequences of missed nodes during retroperitoneal lymph node dissection (RPLND). Retroperitoneal relapse can occur if at least one missed node contains vital cancer, and late recognition of relapse can result if the tumour does not yield any serum tumour marker rise. If the missed node was the only pathologic node in that patient, he will be discharged from the hospital as pathologic stage I. The disease will progress with time, and an easy case may become a difficult one. Repeat RPLND is not an easy operation, and not all germ cell tumour metastases are curable with chemotherapy. 2. Evidence acquisition 2.1. Lymphatic drainage of the testis To avoid missed nodes at RPLND, it is imperative to know the lymphatic drainage of the testis. Lymphatic drainage from the testis to the retroperitoneal nodes was well known more than a century ago. The French surgeon Cune´o gave an accurate description of retroperitoneal nodes (Fig. 1) in 1901 at the Societe´ de Anatomi in Paris, France . He divided superficial nodes (those lateral and anterior to the great vessels) from deep nodes (those behind the great vessels): ‘‘The para-aortic nodes are on both sides of aorta: They drain the lymph from the common iliac nodes and from kidneys and testis (or ovary). Right para-aortic nodes are all around inferior vena cava. Pre-aortic nodes drain the lymph from para aortic nodes and from lymphatics around the mesenteric and celiac arteries. Deep retro-aortic nodes receive the lymph from para-aortic and pre-aortic nodes and drain into the Pecquet’s cisterna chyli, which continues upward with the thoracic duct’’ (Fig. 1). Contemporarily, he and other surgeons [2–4] introduced RPLND en bloc with the spermatic cord and the cancerous testis. Nevertheless, testicular cancer has remained an anecdotal disease since World War II, when >1000 testicular cancers were studied at the Washington Armed Forces Institute of Pathology . So far, the natural history of testicular tumours was widely understood, and Mallis and Patton  moved the field of transperitoneal RPLND for nonseminomatous germ cell tumours (NSGCT). In 1963, Bursch and Sayegh  reported their studies on the visualisation of human testicular lymphatics, combining pedal and funicular lymphangiography. These studies revealed primary zones of spread not shown on pedal lymphangiography. Fig. 1 – Artistic drainage of retroperitoneal lymph nodes by Cune´o, 1901 . Chiappa et al  and Wahlqvist et al  confirmed and added to these observations. Consequently, surgeons started to study the distribution of retroperitoneal lymph node metastases. 2.2. Distribution of retroperitoneal lymph node metastases 2.2.1. Memorial Sloan-Kettering Cancer Center  In 1974, Ray et al  reported the distribution of retroperitoneal lymph node metastases in 122 out of 321 ‘‘explored’’ NSGCT of the testis. For the right testis, the paracaval, precaval, interaortocaval, preaortic, right common iliac, and right external iliac nodes represented the ipsilateral distribution. The contralateral distribution (left testis) was attributed to the para-aortic, preaortic, left common iliac, and left external iliac nodes. Experience with anomalies such as horseshoe kidney, retroaortic left renal vein, and left cardinal vein suggested that such malformations did not materially influence the distribution of the retroperitoneal lymphatic drainage of the testis. In the earlier years, extended bilateral RPLND was performed from ureter to ureter and from renal pedicles to bifurcation of the aorta, including dissection of the common iliac and proximal onethird of the external iliac vessels. Overall, 61 patients on each side had radically resected RPLND metastases: On the right side, 18 patients had metastases in a solitary node and 43 had multiple nodal metastases. On the left side, 17 patients had a solitary metastasis and 44 had multiple metastases. 472 european urology supplements 8 (2009) 470–477 The conclusions were that the lymphatic drainage from the right testis is to interaortocaval, precaval, preaortic, paracaval, right common iliac, and right external iliac nodes. The lymphatic drainage from the left testis is to the para-aortic, preaortic, left common iliac, and left external iliac nodes, in that order. With right-sided tumours, the metastases were to the ipsilateral nodes in 85% of cases, to both ipsilateral and contralateral nodes in 13% of cases, and to contralateral nodes only in 1 case. With left-sided tumours, the ipsilateral nodes alone were involved in 80% of cases and both ipsilateral and contralateral nodes were involved in 20% of cases. 2.2.2. Indiana University  Eight years later, Donohue et al  studied the distribution of nodal metastases in nonseminomatous testis cancer, with particular interest in the suprahilar zone. The distribution of nodal metastases in 104 consecutive pathologic stage II NSGCT patients was analysed and segregated into 11 anatomic zones of spread: (1) right paracaval, (2) right precaval, (3) interaortocaval, (4) left preaortic, (5) left para-aortic, (6) right suprahilar, (7) left suprahilar, (8) right iliac, (9) left iliac, (10) interiliac, and (11) gonadal veins. All patients underwent full bilateral dissection from ureter to ureter and from diaphragmatic crura down to aortic bifurcation and iliac arteries. Tumour deposits in these 11 nodal zones were correlated with the side of the primary tumour (right vs left) and the extent of retroperitoneal metastases: B1, B2, B3 (IIA, IIB, IIC). Lymphatic drainage from the right testis involved interaortocaval, precaval, and preaortic zones, in that order. In no case of early stage disease (B1) was there any suprahilar nodal involvement; however, with more extensive disease, suprahilar nodes were found in up to 33% of the cases. Lymphatic drainage from the left testis revealed a marked predilection for the left para-aortic and preaortic zones in early stage disease and extension to the interaortocaval zone in stage B2 disease. The involvement of only three suprahilar nodes was noted in early stage (B1) disease. Again, with advanced B2 disease, suprahilar nodes were involved much more frequently. Gonadal veins were involved with tumour in 14% of cases on the right side and in 17% of cases on the left. The iliac areas were involved rarely in early stage disease, and contralateral iliacs were not involved except for one case, right to left. No contralateral tumour was seen in early stage disease with the primary site in the left testis, and only one tumour was seen in late-stage disease. Conversely, if the tumour originated in the right testis, contral- ateral involvement did occur in early stage disease and more often in late-stage disease. Suprahilar metastases are extremely rare in early stage disease, and crossover of metastases is clearly prevalent from right side to left. 2.2.3. Testicular Tumour Study Group The third fundamental paper on distribution of retroperitoneal lymph node metastases in NSGCT came from a multicentre German cooperative study , demonstrating that big studies can be performed outside high-volume centres. The aim of the study was to identify the localisation of retroperitoneal lymph node metastases in pathologic stage II NSGCT of the testis to obtain both a safe template for RPLND and to preserve antegrade ejaculation. The study included 214 consecutive patients with pathologically documented retroperitoneal metastases, excluding those with metastases >5 cm. Patients were divided into three groups: group 1 consisted of solitary metastasis; group 2 consisted of 2–5 metastatic nodes with none >2 cm (B1); and group 3 consisted of >5 metastases between 2 and 5 cm (stage B2). Results were evaluated according to metastatic groups and laterality, comparing patients with only one metastatic node to patients with stage-B1 or B2 disease. Also in this study, the crossover of metastases was not seen in patients with only one metastatic node. In contrast, in patients with multiple metastases, the crossover from right to left was more frequent (15%) than the crossover left to right (5%), which was observed only in pathologic stage B2 case. This study confirmed the results of the two preceding studies, with the exception that no one confirmed Ray et al’s  observation of a contralateral solitary metastasis. 2.2.4. Conclusions These three studies confirm that in pathologic stage IIA disease, the crossover left to right is rare, while the reverse—right to left—is more common. Furthermore, looking at anatomy and distribution of metastases, it is also clear that testicular lymphatics do not follow only the vein, as it was believed. The fact that on the right side metastases are more frequent in the interaortocaval region and on the left side they are preferentially distributed between the superior para-aortal region and the renal vein demonstrates that testicular lymphatics follow at a large both vein and artery. Furthermore, the nodes behind the great vessels  have never been mentioned in these three studies. Recently, it has been reported in three papers [13–15] that the major site of nodal recur- 473 european urology supplements 8 (2009) 470–477 rences is retrocaval: All these cases had advanced disease, and if the lumbar veins are not divided, retrocaval metastases will be missed. We need to bear clearly in mind that the inferior vena cava (IVC) is surrounded by the whole package of right paraaortic nodes . The same situation exists on the opposite side when there is the left cardinal vein instead of the IVC. In this situation, anatomy is overturned. It is a matter of fact that the terms interaortocaval, precaval, laterocaval, and retrocaval may be confusing: All of these nodes are right para-aortic nodes. 2.3. Full and modified templates for retroperitoneal lymph node dissection Table 2 – Distribution of retroperitoneal lymph node metastasis in patients with only one metastatic node (sum of template in Ray et al  and Weissbach and Boedefeld ) Anatomical sites Table 1 – Distribution of retroperitoneal lymph node metastases in pathologic stage IIA disease (sum of templates in Donohue et al  and Weissbach and Boedefeld ) Anatomic sites Right side (92 patients) Paracaval Precaval Interaortocaval Preaortic Para-aortic 21 37 55 12 6 (23%) (40%) (60%) (13%) (6.5%) Right iliac Common External Left iliac Hilar/suprahilar 8 1* 3 2* (9%) (1%)* (3%) (2%)* * Refers to Weissbach and Boedefeld  only. Left side (75 patients) – – 2* (2.7%)* 8 (11 %) 24 (32 %) 67 (89 %) – – 3 3 – – (4%) (4%) Left side (55 patients) Paracaval Precaval Interaortocaval Preaortic Para-aortic 7y (13%)y 13 (24%) 24 (44%) 3 (5.5%) –– – 1y (2 %)y 1y (2 %)y 4y (7 %)y 48 (87%) Right iliac Common External Left iliac Hilar/suprahilar 5 (9%) 1z (2%)z –– 1y (2%)y – – 1z (2%)z – y These three studies [10–12] should allow us to define the landing zones and to design templates to avoid unnecessary extended RPLND in early stage disease. No retroperitoneal zone was disease free in pathologic stages IIB and IIC [11,12]. Adding up Donohue et al’s  and Weissbach and Boedefeld’s  reports, right-sided stage IIA tumours had all zones involved by metastases, while three zones on the left sided (precaval and contralateral iliac) were tumour free (Table 1). Considering patients with only one metastatic node [10,12], the distribution of retroperitoneal metastases was unilateral only on the right side, while contralateral metastases (precaval and interaortocaval) were found in two cases of left-sided tumours (Table 2). Recently, Eggener et al  reported on 191 consecutive patients with pathologic stage II NSGCT out of 364 patients with clinical stage I disease and 136 patients with clinical stage IIA disease who underwent RPLND at Memorial Sloan-Kettering Cancer Centre (MSKCC) between 1989 and 2004. Right side (54 patients) z Refers to Weissbach and Boedefeld’s findings only . Refers to Ray et al’s findings only . Teratoma alone was present in 17 of these 191 patients (9%) and in combination with other histologies in other 26 patients (14%). Pathologic stage following RPLND was pN1 in 91 patients (47%), pN2 in 97 patients (51%), and pN3 in only 3 patients (2%). Cure with surgery alone was achieved in 90% of pathologic stage I patients and in 70% of pathologic stage IIA patients. Patients with pathologic stage IIB or IIC disease received adjuvant chemotherapy. The aim of the study was to define the incidence of missed nodes outside five modified RPLND templates, three described for open surgery [10–12] and two for laparoscopic surgery [17,18]. Extratemplate disease ranged from 3% to 23%, including 23% of patients with chemoresistant teratomatous elements. For the right-side templates, inclusion of para-aortic, preaortic, and right common iliac zones would have decreased the incidence of extratemplate disease to 2%. For the left-side template, inclusion of the interaortacaval, precaval, paracaval, and left common iliac zones would have decreased the incidence of extratemplate disease to 3%. In other words, for the right side only left iliac nodes could be omitted; for the left side, only the right iliac nodes could be omitted. Hilar/suprahilar nodes were not considered in this study. How can we introduce these data into clinical practice? Solitary lymph node metastases cannot be predicted, but early stage lymph node metastases are usually found in about 30% of clinical stage I disease and in about 60% of cases in clinical stage IIA disease . Today, RPLND is an option for both clinical stage I and clinical stage IIA disease . Surveillance is favoured in low-risk stage I disease (metastases in 14–22% of cases), and chemotherapy is favoured both in high-risk (vascular invasion) 474 european urology supplements 8 (2009) 470–477 clinical stage I patients (metastases in 48%) and in all clinical IIA cases (metastases in 60% of cases). Post-RPLND loss of antegrade ejaculation has been nearly ‘‘demonized’’ for years, and very few words have been spent to explain the mechanism of loss of antegrade ejaculation and how it can be elegantly avoided. The nerve-sparing technique was introduced by Jewett et al in 1988 : T12–L3 fibres coming from both right and left sympathetic chains converge on both sides of the aorta to form a plexus around the origin of the inferior mesenteric artery. This superior plexus passes over the aortic bifurcation to slide down and reach the inferior hypogastric plexus and the pelvic plexus. The sympathetic fibres are responsible for the closure of the bladder neck during orgasm to avoid antegrade ejaculation (emission is supported by pelvic nerves S2–S3). All sympathetic structures are recognisable and, when they are not adherent to retroperitoneal metastases, they can be identified and prospectively preserved (Fig. 2). Additionally, template dissections can preserve ejaculation, with unilateral RPLND for clinical  or intraoperative  stage I disease or with modified RPLND templates to avoid contralateral nerves. In particular, it has been demonstrated that by preserving only the contralateral L3 fibre at the level of the inferior mesenteric artery antegrade, ejaculation is usually maintained  (Fig. 3). Furthermore, imipramine chloride (a drug used to close the bladder neck for enuresis) helps antegrade Fig. 3 – Bilateral modified template with nerve sparing of contralateral L3 for a right tumour. emission. The difference between prospective nerve-sparing RPLND and template dissection is that the prospective RPLND allows a full bilateral dissection (Fig. 2), while modified template RPLND avoids contralateral dissection and can miss nodes around the preserved nerves. Weissbach and Boedefeld  proposed modified unilateral templates for clinical stage I NSGCT to obtain preservation of antegrade ejaculation sparing the contralateral sympathetic nerves. The templates included the right side, paracaval, precaval, interaortocaval upper preaortic (above the level of the inferior mesenteric artery), and common iliac nodes; on the left side was the para-aortic nodes and upper preaortic nodes. It was a good template to avoid loss of antegrade ejaculation but not so good to avoid missed nodes. According to the distribution of lymph node metastases, it is clear that even in the case of a solitary metastasis on the right side (Table 2), an occasional patient may have metastatic disease. Weissbach and Boedefeld’s templates have been proposed for clinical stage I disease , but they fit only for the great majority, not the totality, of patients. 2.4. Fig. 2 – Bilateral nerve sparing following bilateral retroperitoneal lymph node dissection. Laparoscopic retroperitoneal lymph node dissection Laparoscopic RPLND (L.RPLND) has become a routine approach for pathologic staging of clinical stage I NSGCT of the testis in several centres. L.RPLND is typically performed unilaterally on a modified flank position, and lymph node dissection usually follows european urology supplements 8 (2009) 470–477 the boundaries described by Weissbach and Boedefeld . As L.RPLND was considered a staging procedure, patients with positive nodes are regularly given two courses of adjuvant chemotherapy [24–26]. Recently, Steiner et al introduced the bilateral nerve-sparing L.RPLND technique , and Rassweiler et al produced an excellent review paper comparing L.RPLND to open RPLND (O.RPLND) . Nevertheless, it is impossible to evaluate the curative potential of L.RPLND, as pathologic stage II patients are typically given two courses of adjuvant chemotherapy. When I started to perform L.RPLND in clinical stage I patients, I decided not to give adjuvant chemotherapy to N+ patients, as it was done on open surgery , but the first two patients with positive nodes developed liver metastases in a few months . Nevertheless, in the Rassweiler et al review , of 140 patients with positive nodes (25%) who were to receive adjuvant chemotherapy, 14 did not. Only two of these patients relapsed, but not in the liver. Also, in the German Testicular Cancer Study Group , only 2 out of 10 N+ patients who did not want to receive adjuvant chemotherapy relapsed. Tumour seeding after L.RPLND has been sporadically reported, and in a large review paper, only one case was reported out of 479 L.RPLND cases . L.RPLND seems to be feasible. Also, bilateral laparoscopic nerve-sparing RPLND is technically feasible , and even obese patients can undergo successful L.RPLND . The weak point of L.RPLND seems to be recurrences outside templates [16,24,26,28,35,36], usually following original or modified Weissbach-Boedefeld templates . This is a template deficiency, but it is also the responsibility of the surgeon to trust templates in the presence of metastatic disease at surgery. This topic has been deeply studied in Innsbruck [25,27,37,38]. The researchers first studied whether primary metastatic spread could be behind the lumbar vessels when positive nodes were exclusively ventral to the great vessels in early stage disease, while metastases behind the lumbar vessels were found only in 3 out of 25 patients with multiple metastases . Also, none of the pathologic stage I patients who relapsed after L.RPLND had developed any relapse behind the great lumbar vessels . They also found retrocaval recurrence only in postchemotherapy L.RPLND , as was reported by others [13–15]. 2.5. Postchemotherapy surgery In this era of surveillance in good-risk stage I disease and of primary chemotherapy in all other cases 475 [19,39,40], the recognised role for surgery is postchemotherapy removal of residual disease after primary chemotherapy. The aim of this surgery is to avoid early and late relapses. In two recent and important reports [41,42], viable cancer was present in 12% of patients, mature teratoma in 37% and fibrosis necrosis in 51% of patients in two cumulative series of 684 cases. In the European study , patients were selected for modified template resection or radical template resection on the basis of the prechemotherapy location and size of the residual mass. Radical resection was performed in all cases of contralateral spread, interaortocaval location, or tumour diameter >5 cm; a modified template resection was performed if the prechemotherapy location of the residual mass corresponded to the primary landing zone and the residual mass was 5 cm. Ejaculation was preserved in 85% of patients who underwent a modified template and in 25% of patients who underwent full bilateral resection. After a median follow-up of 39 mo, only eight (5%) patients recurred, three after modified RPLND and five after full template. All patients underwent salvage surgery: Four had teratoma, and three had vital cancer. Another six patients developed systemic disease. In the American study , 210 patients (40%) had teratoma, and 59 patients (11%) had viable cancer. The median follow-up for survivors was 45 mo. Their results were evaluated according to four different templates: Weissbach and Boedefeld , Indiana , Ray et al , and Johns Hopkins University . The incidence of retroperitoneal extratemplate disease ranged from 7% (Ray et al) to 32% (Weissbach and Boedefeld). Furthermore, a German study group realized that postchemotherapy FDG-PET is unable to give a clear benefit in the prediction of tumour viability in residual masses . 3. Evidence synthesis The studies on the distribution of retroperitoneal metastases in NSGCT of the testis were intended to help surgeons to avoid both missed nodes at RPLND and unnecessary extended dissections. Ray et al , Donohue et al , and Weissbach and Boedefeld  correctly analysed the distribution of both single RPLND metastases [10,12] and pathologic stages IIA, IIB, and IIC [11,12]. Excellent laparoscopic surgeons in Innsbruck found the correct surgical approach to L.RPLND  and contemporarily applied the Weissbach-Boedefeld template to L.RPLND for clinical stage I NSGCT . The problem arose when the 476 european urology supplements 8 (2009) 470–477 template dissection became an easy guide to nervesparing RPLND instead of the more difficult and demanding prospective nerve-sparing RPLND first described by Jewett et al . Maintaining antegrade ejaculation seemed to become the priority goal at staging RPLND, nearly to the extent of forgetting that approximately 30% of clinical stage I patients do have metastatic nodes and that approximately 50% of these metastatic nodes are pathologic stage IIB disease . Of course, surgical planning has to be changed during staging RPLND whenever evidence of metastasis occurs. The staging template has to cover pathologic stage IIA disease, which is mainly diagnosed at definitive pathologic examination. According to Table 1 and the Steiner at al paper , a security template for left-sided clinical stage 1 NSGCT should include at least interaorta and left iliac nodes besides para-aortic and preaortic nodes. A theoretical 5% relapse risk remains for precaval and hilar/suprahilar nodes. A security template for right-sided tumours should include all anatomic sites. Including upper para-aortic nodes at least, the risk for the right side will decrease to 4.5%. Only a prospective nerve sparing surgery will allow both radical RPLND and maintenance of antegrade ejaculation. 4. 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