Transperitoneal laparoscopical iliac lymphadenectomy for treatment of malignant melanoma

Surg Endosc (2003) 17: 1536–1540 DOI: 10.1007/s00464-002-9219-6 Ó Springer-Verlag York Inc. 2003

Transperitoneal laparoscopical iliac lymphadenectomy for treatment of malignant melanoma F. Picciotto,1 E. Volpi,2 A. Zaccagna,1 D. Siatis1 1 2

Operative Unit of Surgical Dermatology, Institute for Cancer Research and Treatment, Strada Provinciale 142, Km 3.95, 10060 Candiolo, Italy Department of Gynecological Oncology, Institute for Cancer Research and Treatment, Strada Provinciale 142, Km 3.95,10060 Candiolo, Italy

Received: 10 October 2002/Accepted: 21 March 2003/Online publication: 21 July 2003

Abstract Background: Current treatment for melanoma of the lower limb includes excision of the primary tumor with ilioinguinal lymphadenectomy in the case of lymph node metastases. The standard surgical approach includes sectioning of the inguinal ligament to gain access to the iliac nodes. More recently, some authors have reported that extraperitoneal laparoscopically assisted ilioinguinal lymphadenectomy for the treatment of malignant melanoma is feasible and less aggressive than standard open surgery. So far, no publications have described transperitoneal laparoscopic iliac lymphadenectomy (TPLND). Methods: From November 2001 to June 2002, 13 patients with ilioinguinal node melanoma metastases underwent TPLND (stage IIIA in 1 case, IIIB in 5 cases, IIIC in 4 cases, and IV in 3 cases). Results: In all 13 cases, the TPLND and groin dissection was performed correctly. Operative time, intra- and postoperative complications, number of lymph nodes retrieved, immediate morbidity, hospital stay, and feasibility of TPLND were evaluated. Conclusions: This study was conducted to evaluate the feasibility and the preliminary results of TPLND used to manage malignant melanoma of the lower limb. This approach has many advantages over the traditional procedure: less surgical trauma, no incision of the abdominal muscles or the inguinal ligament, and less postoperative pain. Moreover, as compared with extraperitoneal laparoscopically assisted ilioinguinal lymphoadenectomy, it provides an improved view of the operative area, dissection zone, and surrounding structures. Further research is needed to confirm these preliminary results regarding the potential applications of this method for treating malignant metastasis to the lower limb.

Correspondence to: F. Picciotto

Key words: Ilioinguinal lymphadenectomy — Laparoscopic iliac lymphadenectomy — Laparoscopy — Malignant melanoma — Metastatic melanoma

The standard treatment for melanoma of the lower limb is excision of the primary tumor together with lymphadenectomy in the case of lymphnode metastases [8–24]. When groin lymph nodes are positive, pelvic lymphadenectomy should be performed. The traditional surgical approach generally is groin and extraperitoneal pelvic dissection with resection of the inguinal ligament through a longitudinal incision, although Karakousis’ technique aims to preserve the inguinal ligament through a transverse incision performed parallel and cephaled to the inguinal ligament to gain access to the retroperitoneal space [10]. In recent years, laparoscopic lymphadenectomy has proved to be effective in managing pelvic malignancies in the male [9–28] and female [17, 18]. This study was conducted to evaluate the feasibility and the preliminary results from the association of transperitoneal laparoscopic pelvic lymphadenectomy and standard open groin dissection used to manage malignant melanoma of the leg. Patients and methods Patients From November 2001 to June 2002, 13 patients with melanoma metastases in the ilioinguinal node underwent transperitoneal laparoscopic iliac lymph node dissection (TPLND). Of the 13 patients, eight were women and five were males. Their average age was 56.9 years (range, 28–78), and the clinical stage, according to the new AJCC classification [1, 2], was IIIA in one case, IIIB in five cases, IIIC in four cases, and IV in three cases. In two patients, lymphadenectomy was performed for sentinel node positivity, whereas in all the other cases, lymphadenopathy was clinically evident. In one case, the sentinel node was negative at diagnosis, but palpable adenopathy was present after 3 months.

80 70 75 90 1 0 1 0 2 2 8 14 15 21 31 23 6 10 20 16 9 11 11 7 T2aN1bM0 IIIB T4aN2M1c IVC TxN3M0 IIIB T4aN3M1a IVA Not done Not done Not done Neg

90 0 1 20 11 9 T4bN1bM1b IV

F

F M

F M M F

7

8 9

10 11 12 13

78 48 30 38

75 0 6 19 6 13 T2bN2cM0 IIIC Not done

Not done

SSM IV liv. 1.8 right leg NM on SSM IV liv. 4.2 mm left leg NM IV liv. 1.9 mm right leg MN IV liv. 6 mm right buttock SSM With >80% regression NM V liv. 6 mm sacral

M M F F F 2 3 4 5 6

69

F 1

45 63 65 68 69

Gender Patients

69 70

80 0 1 21 7 14 T3aN1bM0 IIIB Not done

75 70 80 90 75 0 0 4 0 0 1 3 6 0 1 25 23 21 26 23 8 8 6 14 8 17 15 15 12 25 T3bN1bM0 IIIC T4bN1bM0 IIIC T4bN1bM0 IIIC T3bN1aM0 IIIB T4aN1aM0 IIIA Not done Not done Not done Pos Pos

0 1 35 10 25 T4aN1bM0 IIIB

AJCC Sentinel node

Neg

NM on SSM IV liv. 4.9 mm left leg NM IV liv. 3 mm left leg NM V liv. 4 mm right leg NM V liv. 9 mm lombare right NM IV liv. 3.8 mm right leg NM on SSM IV liv. 4 mm right leg NM on SSM IV liv. 3.6 mm right leg

Positive inguinal lymph nodes (not sentinel node) n Total excised (ilioinguinal) inguinal lymph nodes n Excised inguinal lymph nodes n Excised iliac obturator lymph nodes n Primitive melanoma (Clark, Brealow) site

In all 13 cases, the TPLND and groin dissection were performed correctly. No postoperative bleeding occurred, nor was any second procedure necessary. The mean postoperative hospitalization stay was 4.5 days (range, 4–5). The mean duration of the complete procedure (TPLND and groin dissection) was 180 min (range, 150–210). The mean time for laparoscopic lymphadenectomy was 75 min (range, 65–95). The mean number of external iliac lymphnodes removed was 7.8 (range, 6–9), and the mean number of obturator lymph nodes was 6.5 (range, 1–17). The mean number of the pelvic lymphnodes was 14 (range, 9–25). In all the patients, the drain was removed from the pelvis within 48 h, whereas the groin drain was left until

Age (years)

Results

Table 1. Patients who underwent transperitoneal laparoscopic iliac lymph node dissection

All the patients gave informed consent for the laparoscopic procedure. However, the eventuality of conversion to an open procedure was clearly explained. Bowel preparation included a clear liquid diet and a laxative on the day before surgery. Typing and cross-matching was performed in every case. The patients were given antibiotics (cephalosporins) and antithrombotic prophylaxis (low-weight heparins). General anaesthesia and endotracheal intubation are needed for the TPLND procedure. The patients are positioned as for a lithotomy. A gastric probe and a catheter are inserted. A veress needle is used to create the pneumoperitoneum and a 10mm trocar is placed at the umbilicus. In all, four trocars are inserted. One trocar is placed in the umbilicus for optics, and a second 10- to l2mm trocar is placed centrally just above the pubic bone. The sovrapubic trocar generally is disposable to facilitate lymph node extraction. Two 5-mm trocars are placed between the epigastric vessels and the anterior superior iliac spine. After the intestinal bundle is replaced from the pelvis and adhesiolysis is performed, in the female we first open the lateral leaf of the broad ligament. The limit of the opening is approximately 4 to 5 cm over the crossing between the infundibulopelvic ligament and the iliac vessels. In the male, the opening of the peritoneum is performed more distally, identifying the gonad vessels, which are mobilized laterally. In the retroperitoneum, the first structure to be identified is the psoas muscle, and then ureter and iliac bifurcation are detected. In the male, the ductus deferens is preserved, whereas in the female, the round ligament can be severed if more space is needed. We generally complete the identification of all the anatomic limits of the dissection, so we open the paravescical space by grasping the umbilical ligament and pulling it medially (Fig. l). The pubic bone, the obturator nerve, the obturator muscle, and the whole course proximal to the internal iliac artery must be visualized. Lymphadenectomy then begins from the proximal side of the lateral external iliac nodes. The anatomic borders of lymphadenectomy at this step are the epigastric bundle and the inguinal ligament. The adventitia of the vessels is dissected, and the medial iliac external nodes are retrieved. The external iliac vessels are detached from the pelvic wall and separated from each other. All the lymphatic material between the vessels and the pelvic wall is retrieved. Then the lymphatic pad of the obturator fossa is detached from the pelvic wall and collected after further visualization of the obturator nerve. The limits of dissection are anterior to the pubic bone, medial to the external iliac vessels, inferior to the obturator nerve, and posterior to the lumbosacral fossa where the lumbosacral nerve can be identified (Fig. 2). The nodes are retrieved in separate plastic containers according to the area of collection.

Positive iliac obturator lymph nodes n

Preparation and laparoscopic technique

28

Operation time (min) (laparoscopse)

Clinical staging was performed in all the patients before surgery using total body tomography. In all cases, the Karnofsky index was higher than 80%, and no patients had abnormal S-100 or lactate dehydrogenase blood levels. These data are summarized in Table 1.

75

1537

1538

Fig. 1. Grasping the umbilical ligament and pulling it medially.

Fig. 2. Lumbosacral nerve.

lymphatic secretion decreased to between 20 to 30 ml/ day. We observed only two complications. The one was related to the laparoscopy procedure and involved hypercapnia and subcutaneous emphysema that regressed within 2 days. The other was a wound diastasis.

distributed along the length of the iliac and femoral vessels in two distinct anatomic regions: the iliac region, which is intraabdominal, and the inguencrural region, which is extraabdominal. There are about 10 to 20 lymph nodes in the inguencrural region, and there are about 6 to 8 along the iliac vessels, whereas in the obturator fossa, the number varies from 3 to 4 [3, 12, 26]. Access to the iliac obturator area in traditional surgery is difficult mainly because of the inguinal ligament. Incision of the inguinal ligament gives rise to postoperative complications such as hernias [16]. Therefore, many techniques have been proposed for access to the iliac lymph nodes that conserves the inguinal ligament [10]. However many authors, to ensure radical surgery in oncologic terms, prefer to resect the iliac obturator lymph nodes by sectioning the inguinal ligament and large abdominal muscles via a vertical incision about 3 cm medially for approximately 10 cm above the anterior superior iliac spine [26]. Laparoscopy to remove iliac obturator lymph nodes in patients with melanoma of the leg has been described in the literature. It seems to offer some advantages in terms of collateral effects and hospitalization equal to those of radical oncologic surgery, as compared with traditional surgical techniques [25]. However, the literature describes only extraperitoneal laparoscopy for the management of malignant melanoma of the leg [25], and no publications yet foresee surgery via transperitoneal laparoscopic iliac lymphadenectomy. The technique for transperitoneal laparoscopic iliac lymphadenectomy described in this report may offer some advantages over the classical retroperitoneal laparoscopic approach. First, better anatomic visualization allows a safer radicality in the operation, an essential element in treating metastatic melanoma. Furthermore, this radicality (8 excised lymph nodes) is completely comparable with both the traditional approach and retroperitoneal laparoscopy (in the number of lymph nodes) [25]. Finally, the operation times are lower than for any other surgical technique described so far when performed by expert hands.

Conclusion Transperitoneal laparoscopic iliac lymphadenectomy is technically feasible also for metastatic melanoma of the lower limb in combination with groin dissection. This approach has many advantages over the traditional procedure: less surgical trauma, no incision of the abdominal muscles or the inguinal ligament, and less postoperative pain. The postoperative hospital stay was shorter than for the traditional procedure (mean postoperative stay, 18 days) [23], and similar to that reported by Pearlman et al. [16] for a modified ilioinguinal node dissection (paired oblique skin incision 4–5 cm above and below the inguinal ligament), and to that reported by Janetschek et al. [9], who performed laparoscopic retroperitoneal lymph node dissection (mean postoperative hospital stay, 3.3 or 3.5 days). The number of pelvic lymph nodes retrieved by laparoscopic surgery was as expected. We believe that TPLND allows good surgical radicality, similar to that of the traditional technique, with less surgical morbidity. Discussion Superficial groin dissection is defined as removal of the nodes from above the inguinal ligament to the apex of the femoral triangle, skeletonizing in this process the femoral vessels and nerve. Ilioinguinal node (radical groin) dissection is defined as removal of these nodes plus the iliac and obturator nodes [4, 10, 11]. Radical groin dissection therefore involves more lymph node groups, to a total of approximately 20–30 lymph nodes

1539

With respect to iliac obturator excision by traditional means, the advantages are comparable with those reported for surgical retroperitoneal laparoscopy: reduced surgical trauma, fewer pain symptoms, lower morbidity, shorter hospitalization stays, and better aesthetic results. As for contraindications, the potential dysrhythmogenicity of hypercapnia may contraindicate the extraperitoneal approach in patients with cardiopulmonary disease [7], and in patients with lower extremity joint protheses [5]. Obesity is not a contraindication for laparoscopic pelvic lymph node dissection [20]. Previous laparoscopy could, on the other hand, make surgery more difficult from a technical point of view. The complications of transperitoneal laparoscopic iliac lymph node dissection are well known and include all of the complications associated with laparoscopic surgery: vascular and visceral injuries that require open conversion, risk of lesions to the ureters when surgery is near the iliac bifurcation, and difficulty controlling bleeding by the obturator vessels or the iliac vein. It is important to remember that most complications occur in the initial phases of surgery [13]. The postoperative complications involve predominantly thromboembolism, wound infection at trocar sites, hematomas, urinomas, urinary infections, and pulmonary disorders [21, 22]. Lymphoceles are rarely reported after laparoscopic pelvic node dissection [6]. In our experience, transperitoneal laparoscopically assisted ilioinguinal lymphadenectomy does not appear to reduce the number of these complication, as compared with traditional surgery. Objections to laparoscopic TPLND focus on the longer operative time and the increased operative cost, as compared with open surgery, although these are compensated by a shorter hospitalization stay [29] and a total cost that may be similar or even lower [15]. According to the authors, an increase in experience reduces surgery times and thus the risk of complication. It also reduces costs. A further criticism of laparoscopy is represented by the possibility of performing a ‘‘not oncologically correct’’ operation. However, our experience leads us to believe that the number of excised lymph nodes makes it suitable to consider this method radical. The average number of excised iliac obturator lymph nodes is 14. The final problem is neoplastic recurrence in trocar implant sites resulting from direct contamination during extraction of the contaminated piece [19, 27]. To avert neoplastic dissemination, it is advisable to excise the whole lymph node chain in one single operation to avoid excessive manipulation. The main problem with TPLND is surely the long and steep learning curve for surgeons who are used to traditional methods. This is very relevant because the number of complications occurring during this type of surgery could discourage its wide use, depending on the surgeon. The authors maintain that such a technique can offer numerous advantages over the traditional method, with complete respect to the principles of oncologic radicality, allowing lymph node excision to be performed technically similar to traditional methods.

In the literature, the extraperitoneal approach with limited excision space, is reported. We described the transperitoneal approach, which offers better vision in the operating field, optimal visualization of the excision area and surrounding structures, allowance for appropriate instrument maneuvring, easy excision, good control of blood vessels, and, where necessary, rapid conversion to the traditional open method. The risk of metastasis via the entry routes, already described after laparoscopic resection of colorectal cancer, and the presumed effect of malignant cells in the peritoneum by gaseous insufflation still are the object of controlled experimental and clinical trials. Currently, this calls for a prudent approach in the case of malignant lesions. For this reason, we prefer using this method in patients who have positive inguinal sentinel lymph nodes with no evidence of metastatic involvement of iliac obturator lymph nodes at preoperative staging (CT, MRI [magnetic resonance imaging]). Certainly, the potential and applicability of this technique in treating metastatic melanoma of the lower limb can be evaluated out definitively only after randomized studies involving large numbers of participants and long follow-up evaluations. References 1. Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, Fleming ID, Gershenwald JE, Houghton Jr A, Kirkwood JM, et al. (2001) Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 19: 3635–3648 2. Balch CM, Cascinelli N (2001) The new melanoma staging system. Tumori 87: S64–S68 3. Balch CM, Milton GW (1985) Management of regional metastatic melanoma. In: Lippincott JB (Eds) Cutaneous melanoma. Philadelphia, pp 98–106 4. Baronofsky ID (1948) Techinique of inguinal node dissection. Surgery 24: 555–567 5. Cooper CS, Donovan JF, Terrell RB, Cohen MB, Winfield HN (1997) Hip and knee replacement as a relative contraindication to laparoscopic pelvic lymph node dissection. J Urol 158: 128–130 6. Freid RM, Siegel D, Smith AD, Weiss GH (1998) Lymphoceles after laparoscopic pelvic node dissection. Urology 51(5A Suppl): 131–142 7. Glascock JM, Winfield HN, Lund GO, Donovan JF, Ping ST, Griffiths DL (1996) Carbon dioxide homeostasis during transperitoneal or extraperitoneal laparoscopic pelvic lymphadenectomy: a real-time intraoperative comparison. J Endourol 10: 319– 323 8. Harris MN, Shapiro RL, Roses DF (1995) Malignant melanoma: primary surgical management (excision and node dissection) based on pathology and staging. Cancer 75: 715–725 9. Janetschek G, Peschel R, Hobisch A, Bartsch G (2001) Laparoscopic retroperitoneal lymph node dissection. J Endourol 15: 449– 453 10. Karakousis CP (1981) Ilioinguinal lymph node dissection. Am J Surg 141: 299–303 11. Karakousis CP (1998) Therapeutic node dissections in malignat melanoma. Ann Surg Oncol 5: 473–482 12. Karakousis CP, Driscoll DL, Rose B, Walsh DL (1994) Groin dissection in malignant melanoma. Ann Surg Oncol 1: 271–277 13. Kavoussi LR, Sosa E, Chandhoke PS, Chodak G, Clayman RV, Hadley HR, Loughlin KR, Ruckle HC, Rukstalis D, Schuessler W (1993) Complications of laparoscopic pelvic lymph node dissection. J Urol 149: 322–325 14. Kozlowski PM, Winfield HN (2000) Laparoscopic lymph node dissection: pelvic and retroperitoneal. Semin Laparosc Surg 7: 150–159

1540 15. Lecuru F, Taurell R (1998) Transperitoneal laparoscopic pelvic lymhadenectomy for gynecologic malignancies. Surg Endosc 12: 1–6 16. Pearlman NW, Robinson WA, Dreiling LK, McIntyre Jr RC, Gonzales R (1995) Modified ilioinguinal node dissection for metastatic melanoma. Am J Surg 170: 647–650 17. Querleu D (1993) Laparoscopic paraaortic node sampling in gynecologic oncology: a preliminary experience. Gynecol Oncol 49: 24–29 18. Querleu D, Leblanc E (1999) Transumbelical pelvic lymphadenectomy. Laparoscopic surgery in gynaecological oncology. Blackwell Science, Oxford, pp 17–26 19. Schaeff B, Paulucci V, Thomopoulos J (1998) Port-site recurrences after laparoscopic surgery: a review. Dig Surg 15: 124–134 20. Scribner Jr DR, Walker JL, Johnson GA, McMeekin DS, Gold MA, Mannel RS (2002) Laparoscopic pelvic and paraaortic lymph node dissection in the obese. Gynecol Oncol 84: 426–430 21. Soulie M, Salomon L, Seguin P, Mervant C, Mouly P, Hozneck A, Antiphon P, Plante P, Abbou CC (2001) Multiinstitutional study of complications in 1,085 laparoscopic urologic procedures. Urology 58: 899–903 22. Soulie M, Seguin P, Richeux L, Mouly P, Vazzoler N, Pontonnier F, Plante P (2001) Urological complications of laparoscopic sur-

23. 24. 25.

26. 27.

28. 29.

gery: experience with 350 procedures at a single center. J Urol 1656 Pt 1: 1960–1963 Sterne GD, Murray DS, Grimley RP (1995) Ilioinguinal block dissection for malignant melanoma. Br J Surg 82: 1057– 1059 Stone CA, Goodacre TEE (1995) Surgical management of regional lymph nodes in primary cutaneous malignant melanoma. Br J Surg 82: 1015–1022 Trias M, Targarona EM, Piulachs J, Balague C, Bombuy E, Espert JJ, Moral A, Castel MT (1998) Extraperitoneal laparoscopically assisted ilioinguinal lymphadenectomy for treatment of malignant melanoma. Arch Surg 133: 272–274 Veronesi U (1989) Trattato di chirurgia oncologica, vol 2. UTET Torino, Italy, pp 783–795 Whelean RL, Sellers GJ, Allendorf JD, Laird D, Bessler MD, Nowygrod R, Treat MR (1996) Trocar-site recurrence is unlikely to result from aerosolization of tumor cells. Dis Colon Rectum 39(19 Suppl): S7 Winfield HN, Donovan JF, See Wa, Loening SA, Williams RD (1991) Urological laparoscopic surgery. J Urol 146: 941–948 Winfield HN, Donovan Jr JF, Troxel SA, Rashid TM (1995) Laparoscopic urologic surgery: the financial realities. Surg Oncol Clin N Am 4: 307–314