Extraperitoneal Laparoscopic Aortic Lynphadenectomy in Gynecological Cancer

Introduction

A fundamental principle in the assessing the prognosis of many gynaecological cancers such as cancer of the breast, cervix and endometrium is to have information about lymphatic invasion. These tumours spread predominantly by lymphatic channels (Salvat et al,1999)

Whatever the accuracy of the biologic assessment of the tumor aggressiveness, knowing precisely the spread of the cancer at the time it is detected and before the therapy is planned will remain a tremendous necessity. Imaging techniques have improved during the past years and surely will improve again. However nothing can replace the accuracy of the surgical staging.

Nevertheless  cost benefits balance of staging surgery is questionable. The surgery itself is source of morbidity. The postoperative loco regional alterations are cause of decreasing of both efficacy and tolerance of the so called adjuvant therapies (which are destined to be the primary therapies in advanced cancers). Staging surgery can only be accepted if its aggressiveness can be reduced. Videoendoscopic techniques are likely to fulfill this condition while improving the accuracy of the lymphatic invasion assessment. In fact, in advanced lesions when treatment is to be by radio- or chemotherapy, endoscopic surgery gives information about lymph node involvement. Limited surgery such as vaginal hysterectomy is less aggressive with less risk of thromboembolism but gives no information about lymph node invasion (Salvat et al,1999). The current trend is for the treatment of gynaecological cancer to evolve towards minimal access surgery for maximal benefit.

Imaging in the Assessment of Tumor Spread of Cervical Cancer

Imaging techniques aim to assess the spread of the tumor : local spread and lymph glandular spread. Three techniques can be used.

Lymphoangiography (LAG) has been the historical method of choice for the evaluation of the pelvic and aortic lymph nodes. Diagnosis of metastatic disease by LAG relies on the presence of distortion of normal lymph nodes architecture. Diagnosis of lymph nodes metastases by computed tomography (CT), magnetic resonance (MRI) and ultrasonography relies on nodal enlargement. Both LAG and CT have limitation in the detection of lymph nodes metastases.

Heller et al(1990) evaluated the detection of paraortic lymph nodes metastases by ultrasound CT and LAG in patients with cervical cancer. Imaging results were confirmed by surgical staging in all patients. The LAG was found to be the most sensitive for detecting paraortic lymph nodes metastases. The sensitivity and specificity of LAG were 79 % and 73% vs 34% and 96% for CT and 19%and 99% for ultrasonography.

Meta-analysis (Scheidler at al, 1997) compares the utility of LAG, CT and MRI in the detection of pelvic and paraortic lymph nodes metastases in patients with cervical cancer. A total of 17 studies on LAG gathered between 1971 and 1992 ( 1408 patients), 17 studies on CT gathered between 1980 and 1995 (1042 patients) and 10 studies on MRI gathered between 1988 and 1997 (837 patients) were included and used for meta-analysis. The authors concluded that the three imaging studies show no significant differences in the detection of lymph nodes metastases in cervical cancer.

There is however a trend to better global performance for MR imaging than for LAG and CT. This trend appears independent of stage of disease and lymph nodes location (pelvic or aortic). LAG is likely to be the more sensitive method. CT and MRI are less sensitive but more specific. For these reasons and because it enables to assess in the same time local primary tumor volume and extend CT and, moreover, MRI are considered by the authors as the choice imaging methods. Another argument is LAG is more ‘aggressive’ and, what’s more, time consuming.

Position emission tomography (PET) with glucose analogue (FDG) has been recently studied for detection of lymph node metastases in patients with cervical cancer. PET is an imaging method that depends on metabolic rather than anatomic alterations for detection of disease. The metabolic basis exploited for the oncological applications of FDG-PET is the increased glycolysis demonstrated by most neoplastic cells (xxx).

Rose et al(1999) recently evaluated 32 patients with cervical cancer with FDG-PET. This study demonstrated that FDG-PET had the sensitivity of 75 % and a specificity of 92 % in detecting paraortic lymph node metastases. Similar results were recently reported (Grigsby et al, 1999) on 11 patients evaluated  for lymph node metastases. In this study PET technique was compared with CT and LAG. This study, as a previous one, is likely to demonstrate that FDG-PET is, in the detection of lymph node metastases, more accurate if compared with conventional imaging methods.

In the contemporary state of the art it is clear that imaging, while giving excellent results, does not enable the gynaecologist to exclude the presence of lymph node metastases before undertaking the treatment. Non-invasive imaging  techniques are useful in the initial assessment of the patient with cancer but only if they give positive results and in the decision making  of surgical and anaesthetic fitness for surgery. The only reliable test of lymph node invasion is histological examination of the excised nodes and this remains the gold standard. Surgery has a part to play in therapy but, as already stated,  the risk of complications is significant.

Staging Laparotomy in the Management of Cervical Cancer

Surgical staging in gynecology began officially in 1970  when Nelson reported at the First Annual Meeting of the Society of Gynecologic Oncologists, 13 cases of staging laparotomy in stage II B – III cervical cancer. 

His experience  was published in 1977, the rate of aortic metastasis was 16 % (5/31 for the patients at the stage II B) and 46 % (13/28) at the stage III.  

Buchbaum in 1972 reported his experience on 11 patients at stage II B and 20 patients at stage III. The rate of aortic lymph node metastases was 9 % at stage II B and 35 % at stage III respectively. Averette (1972) and then Lagasse (1980) reported a rate of 22 % and 32 % of aortic metastases at stage II B and of 20 % and 31 % at stage III respectively. These data opened the discussion about the usefulness of staging laparotomy in cervical cancer in order to modulate radiation therapy (extended fields ?).

However no direct impact on survival was reported by Nelson himself. The survival rate was 64.5 % of the 31 patients of stage II B who underwent staging laparotomy compared to 92.8 % of  the 14 patients not explored by surgical staging. In the same study the survival rate was 57.8 % of the 28 patients at stage III explored by laparotomy compared to 60 % of the 10 patients not explored by laparotomy (Nelson, 1977). Because of these first not promising results most surgeons renounced to the staging laparotomy. Nevertheless some of them proceeded in this direction. Holcomb et al reported in 1999 a statistically significant improvement in the medial survival on 89 patients submitted to staging laparotomy compared to 172 patients not explored by laparotomy (29 months versus 19 months respectively).

Unfortunately, all the studies concerning the topic are biased. In the studies demonstrating that patients submitted to staging laparotomy do better a bias of selection can be evocated : the patients are in better general conditions in most cases. In studies demonstrating the opposite, it can be argued that the stages II B or III of the non staged population include a lot of stage I while in the staged population they are true stage II B and III. Theoretically, staging surgery can not be questioned. But on the practical point of view the benefit to gain by staging surgery is less than the price to pay.

In fact, the rate of complications in patients submitted to radiation therapy is elevated in surgically assessed patients (Nelson, 1977). The retroperitoneal approach could be an answer to reduce the extension and severity of  the post operative adhesions, with consequential less reduction in the mobility of the intestine. This approach significantly reduces the complication rate : the rate of radiation enteritis grade 3 was 15.3 % after extra peritoneal laparotomy versus 20.1 % after intra peritoneal laparotomy in the GOG prospective and randomized assay (Weiser et al, 1989).

Place of Laparoscopic Staging in Cervical Cancer

Considering the complication rate and cost of laparotomy for aortic lymphadenectomy, some investigators recently explored the feasibility of laparoscopic staging. Evidence of a major reduction in adhesions formation rate after laparoscopic lymphadenectomy compared with transperitoneal laparotomy is available in experimental randomized studies (Lanvin et al, 1997; Chen et al, 1998). Moreover laparoscopic dissection is superior to extraperitoneal laparotomy as far as abdominal adhesion formation is concerned.

The role of laparoscopic staging in cervical cancer is different considering tumors less than 4 cm (early stages) from tumors 4 cm and larger (advanced stages).

Early stages

Even if surgery and radiotherapy afford the same chances of survival in the treatment of early cervical cancer (Landoni and Maneo, 1997), the first is, by most of the gynecologic oncologists, preferred especially in young patients. For the oncologists who prefer the use of  radiotherapy,  knowing the status of the regional lymph nodes is of cardinal importance.

For those who prefer surgery the previous assessment of the nodes could lead to the use of less aggressive surgical techniques (vaginal radical hysterectomy or laparoscopic radical hysterectomy). In any case, the patient assessment always has to start with imaging. If CT (and/or MRI) detects enlarged nodes, they must be assessed by guided biopsy. If this biopsy reveals metastatic involvement, laparoscopy does not have to be performed. If the biopsy is negative, laparoscopy should be undertaken. It is still possible during laparoscopy, to encounter obviously metastatic nodes. Even if technically possible, the laparoscopic dissection of these metastatic nodes should not be undertaken because of the hazards of dissemination. Two choices are possible:  radiotherapy after fine needle aspiration or opened debulking combined or not with radical hysterectomy and/or radiotherapy.

If metastases are not found vaginal radical hysterectomy can be elected as management for the primary tumor. For small tumors laparoscopic assisted radical trachelectomy, a variant of the Schauta Stoeckel radical hysterectomy. can be proposed (Dargent et, 2000). This operation preserves the fertility (Dargent, 2001).

The outcomes for laparoscopic vaginal surgery in the management of early cervical cancer are still poorly documented. In our series the 5 years disease-free survival rate (median follow-up of 52 months) are 100 % for tumors less than 2 cm, 79.2 % for tumors 2 to 4 cm and 50.5 % for tumors more than 4 cm.

Advanced stages

Recurrences in advanced cervical cancer are mostly in the abdominal cavity, either extraperitoneally (aortic nodes) or intraperitoneally. The systematic extended-fields radiotherapy, because of severe complications, is not the solution ( Cunningham et al, 1991). It should be limited to adequately selected cases.

Laparoscopy is the best minimal invasive technique to select for these patients. Peritoneal cytology and the evaluation of the aortic nodes status can be laparoscopically performed. The state of the pelvic lymph nodes does not modify the policy of pelvic irradiation. An additional benefit of pretherapeutic laparoscopy is the possibility of performing ovarian transposition in non menopausal women.

SUMMARY OF INDICATIONS TO LAPAROSCOPIC LOMBOAORTIC LYMPHADENECTOMY and treatment flow-charts

1. Early cervical cancer

2. Advanced cervical carcinomas

Extraperitoneal  lomboaortic lymphadenectomy is performed to evaluate cancer metastasis in order to determine the most appropriate modalities and the extensiveness of the treatment to be applied concerning radiation therapy in particular.

This evaluation is proposed only if routine abdomino-pelvic MRI does not reveal major tumoral invasion.

Extraperitoneal  lomboaortic lymphadenectomy includes:

Transumbilical diagnostic laparoscopy

• Laparoscopic extraperitoneal lymphadenectomy (only if the results of the previous steps are normal)

The indications are as follows :

Stage IB2, IIB, III, IVA (or operable or not operable centro-pelvic recurrence).

Lymphadenectomy precludes systematic extended-field radiation therapy and the associated risk of radiolesions if the lymphnodes have not been invaded. If nodes are positive, it rules out surgery that is probably ineffective.

In cases of macroscopic invasion at this level ,the left supraclavicular lymph nodes are evaluated at the same time. If these lymph nodes have been invaded a stage IVB cancer is diagnosed, requiring chemotherapy.

Radiation therapy is becoming palliative in this instance.

3. Early invasive ovarian carcinomas (apparent stage I).

Staging of early invasive ovarian carcinomas, usually detected after routine laparoscopy for apparent benign lesions,  systematically includes a thorough peritoneal exploration with staged biopsies, infracolic omentectomy, appendectomy, and bilateral pelvic, iliac and paraortic lymph node dissection.

If invasion has occurred, the classification changes from stage I to stage III , and chemotherapy is indicated (Leblanc et al,2000).

The extraperitoneal approach is reserved for the  paraortic dissection, especially in moderately obese patients. The next steps of the staging are performed via the classical transumbilical way.

4. Ovarian cancers with optimal debulking surgery without previous lymphadenectomy

After 6 month chemotherapy, a retroperitoneal lomboaortic lymphadenectomy is feasible.

Contraindications

• Extreme obesity (BMI >30)
• Previous history of retroperitoneal dissection
• Preoperative imaging or diagnostic laparoscopy revealing massive para aortic lymph node invasion, visceral metastases or peritoneal carcinomatosis

General basis

The accepted rules for the investigation and treatment of cancer and the principles of endoscopy must be respected. Lymph nodes usually lie close to vessels, nerves and, sometimes, viscera.. The vascular envelope is invaded late in the process of metastasis and, until invasion occurs, it is safe to remove the nodes. However, once the invasive process reaches the vascular tissue, dissection is no longer possible and small biopsies are the only safe method of obtaining information. Nodes and lymphatic chains should be dissected en bloc to provide an accurate anatomo-pathological assessment. Parietal grafting may be necessary to cover the defect. Care must be taken with extraction of the specimen to avoid spillage of malignant cells - the lymphatic fluid in the node may contain metastatic deposits. Cutting lymph nodes is potentially dangerous for the same reason. The surgeon must be highly skilled and practice both endoscopic oncological surgery regularly. Facilities must be available to convert to open surgery in any complication or untoward incident arises.

Equipment

All the OR equipment and instruments must be regularly maintained in good working order. The instruments should include:

• one 11mm  laparoscopic trocar with pneumostatic device (Blunt Tip®Braun) for the telescope
• two 5mm trocars for the dissecting instruments
• one 10 or 12mm trocar for extraction of nodes
• a "Dargent's celio-extractor" (Lepine Lyon, France) or a 5mm grasping forceps which can be inserted through a 12mm trocar

Preoperative period

Low molecular weight heparin at an isocoagulant dose.
Injection of broad-spectrum antibiotics.

Principles

A preliminary examination under anaesthesia should be performed, the results of pre-operative investigations should be checked to confirm the indications and limitations of the proposed procedure. The retroperitoneal lomboaortic lymphadenectomy achieved via a left internal iliac approach (Dargent et al, 2ooo). The left side is chosen for this approach because most of the lymphnodes are found in the left paraortic region (Michel et al,1998) and because it is also possible to dissect on the right side via this approach (Dargent et al, 2000).If the preoperative work-up reveals right side adenopathy, a similar approach on the right is entirely possible.

Patient Setting

General anaesthesia
Urinary catheter
Gastric tube
Supine position
Torso on the left edge of the table
Flat on the table with a slight right rotation.

Team

The surgeon is on the left of the patient.
The assistant is to the surgeon’s left.
The scrub nurse is to the assistant left.

Trocar placement

*Windows Media Player is required to view videos

Pathological Examination

Immediate pathological examination of all tissues is useful. The nodes must be numbered for identification and the source of each sample recorded to allow correct evaluation.

Surgical Technique

As for pelvic lymphadenectomy, the laparoscopic aortic lymphadenectomy was historically performed transperitoneally. Later on, since 1994, the extraperitoneal approach was proposed.

Such access  has such clear advantages which  deserves to be considered as the standard : in fact, the extraperitoneal approach has the advantage of significantly decreasing the chances of intraperitoneal adhesions. Therefore in cases where leaving no adhesions is crucial, for example in cases where radiotherapy is scheduled, the use of the extraperitoneal approach is recommended.

The first step of the operation consists in a traditional transumbilical transperitoneal trocar insertion which is recommended to thoroughly inspect the abdominal cavity, to perform an abdominal washing, if necessary and to check, once the  extraperitoneal dissection has started, its visualization to prevent the entry of  the peritoneal cavity.

The extraperitoneal approach to the aorta can be obtained using a 3 cm long incision made at the Mac Burney’s point or better, at the point exactly opposite on the left side of the patient, close to the left iliac spine.

The successive layers of the abdominal wall are incised including the fascia parietalis but paying attention to keep the serosa and fascia of the parietal Once the fascia parietalis is opened, the surgeon introduces his forefinger into the pre-peritoneal space and starts veloping the extra-peritoneal space under the guidance of the transumbilical laparoscope, following the psoas muscle upwards.

The  psoas muscle is the first landmark chosen because it has an easily identifiable contour.

The second landmark is the iliac crest which is followed laterally in order to open the inferior part of the space. As soon as the preparation of the space has been initiated a laparoscopic trocar with pneumostatic device (Blunt Tip®Braun) is introduced through the iliac incision. Once the extraperitoneal insufflations has started, the gas is expelled from the peritoneal cavity and  the extraperitoneal laparoscopic assessment can begin.

The cannula is used as a dissector to free the upper part of the left side. As soon as the retropneumoperitoneum is well established, the ancillaries trocars can be introduced. We use to insert them along the mid axillary line.

An entry point is selected in the supra iliac area at the mid axillary line with palpation, fine needle testing puncture

and finally introduction of the first ancillary trocar. This trocar accommodates the laparoscopic dissecting forceps which are used to develop the extraperitoneal spaces upwards to the level of the lower ribs. During these  preliminary step of the operation,  the video-monitor has to be positioned at the head of the operating table on the side of the patient where the surgeon is standing.

For the following steps of the operation the video- monitor is positioned on the side of the patient opposite to the side where the surgeon is working on.

The first landmark is the aponeurosis of the psoas muscle . Detaching the peritoneum from the muscle reveals the ureter, which is the second landmark, then the ovarian vein which is third landmark – a fragile structure which has to be handled with care.

Once the peritoneum has been push medially and the ureter ventrally, the common iliac vessels can be identified and the aortic dissection may start.

The lateral aspect of the aorta is approached in a caudal to cranial direction. At the level of the origin of the inferior mesenteric artery

The dissection is difficult due to the presence of the lower mesenteric autonomic nervous plexus.

There are no drawbacks in dividing this plexus in a female. Once the nervous plexus has been divided and the ventro-lateral aspect of the aorta freed, the dissection is driven cranially up to the level of the left renal vein.

At this point the lymphadenectomy can be carried out

Starting with the right side dissection, the anterior aspect of the vena cava and the inter-aortico-caval space where the  right latero-aortic nodes are lying are cleaned out but it is impossible to reach the opposite aspect of the aorta. Conversely, if the dissection is started on the left side it is perfectly possible, after having cleaned the left lateral aspect of the aorta, to get the right lateral aspect while passing underneath the aorta. Hence it is recommended to start with the left side and move to right side only if difficulties arise.

In the unilateral left side technique the dissection of the left aortic nodes is made either from cranially to caudally or vice versa. The nodes are located between the artery and the psoas muscle and by separating this structures, the lumbar sympathetic chain and the vertebral vessels are revealed.

Once the left aortic lymph nodes have been retrieved, the surgeon moves to the retro-aortic space.
The aorta is separated from the common ventral vertebral ligament.

The aim of this elevation is not only to remove the few nodes lying in the retro-aortic space, but mainly to get access to the right side of the aorta and the inter-caval-aortic space.

This dissection can be made in the spaces located between the successive lumbar arteries although it has to be underlined that the access to the inter- caval-aortic space is limited. It is better to divide the collaterals of the aorta : the fifth lumbar arteries in all cases and the fourth as well if it is needed.

Such a division widely opens the retro-aortic space and enables removal of the right aortic nodes. It also enables to go further via the retro-caval or the precaval routes, and to reach  the space alongside the right aspect of the vena cava.

There are only a few nodes in this area which are generally not a site of metastases except in presence of a right ovarian tumour. Thus apart from cases of ovarian cancer there is no need to go so far if the caval dissection appears, arriving from the left side, dangerous (plexoid disposition of the vertebral veins).

Results

The results of endoscopic surgery must be at least as good as those from conventional surgery. The same number of nodes should be removed and the same outcome in terms of relapse-free survival time, local or regional recurrence, etc should be obtained. Additionally the post-operative recovery should be equivalent or improved.

Vasiliev was the first to publish data about the paraortic lymphadenectomy performed with the laparoscope using a left incision and following the extraperitoneal route. In the four cases he reported the average number of nodes was five: the dissection was limited to the infra-mesenteric area. In the Querleu and Dargent’s series  concerning 53 patients operated on between April 1996 and September 1998 (Querleu et al, 2000) the procedure could be carried out in 51 patients among which nine were found out to have macroscopically positive nodes. These patients were not managed any longer with the  laparoscope. As a consequence 42 patients only were submitted to the laparoscopic dissection. The mean duration of the procedures was 125.9 ±31.8 minutes and the average number of  nodes was 20.7. A preoperative complication occurred in one patient : lateral injury to the ureter managed with stenting. A postoperative complication occurred in three patients : three symptomatic lynphoceles of which one required a drainage under ultrasound and one haematoma causing ileus but leading not to reintervention. One more complication was observed postoperatively :  umbilical incisional evisceration with bowel obstruction. This patient was submitted postoperatively to extended fields radiotherapy and suffered from radiation enteritis. The same was observed in one other of the 16 patients submitted to the same radiation regime.  This patient had an uneventful post-laparoscopic course. No actinic complication was observed for the 34 patients submitted to pelvic radiotherapy.

Starting in 1996, given the evident advantages, we have used mostly the left extraperitoneal approach which was feasible on 82 patients. In 9 cases the approach was transumbilical due partially to the primary cancer and anatomical conditions and in 14 was bilateral extraperitoneal.

The indications were early cervical cancers, pelvic node positive (4 cases), advanced cervical cancers or recurrences, and restaging of ovarian cancers in 6 cases for a total of 111 patients.

of 111 patients, we had to renounce to laparoscopy in 1 case for thick peritoneal adhesions and in three for evident peritoneal involvement. Conversion to laparotomy was due in four cases.

The mean of the harvested nodes was 16.4 (range 4-40) which is completely comparable with the results after laparotomic lomboaortic lymphadenectomy.

From preliminary data seems that the extraperitoneal approach allows a better protection of the bowel loops being maintained intact the peritoneal sac. This condition guarantees fewer adhesions formation decreasing the risk of post actinic enteritis which in our series in only 3 % of cases. Further studies with larger patient series and longer follow-up will be required to assess the tolerance of the combination of Extraperitoneal Laparoscopic Paraortic Lymphadenectomy with extended field radiotherapy.

References:

Reprinted with kind permission from TheTrocar.com

References

1. Averette HE, Dudon RC , Ford JH jr. Exploratory celiotomy for surgical staging in cervical carcinoma. Am J Obstet Gynecol 1972; 113: 1090- 1096. (Medline)

2. Buchbaum HJ. Extrapelvic lymph node metastases in cervical carcinoma. Am J Obstet Gynecol 1979; 133: 814- .

3. Chen MD, Teigen GA, Reynolds HAT et al. Laparoscopy versus laparotomy: an evaluation of adhesion formation after pelvic and paraaortic lymphadenectomy in a porcine model. Am J obstet Gynecol 1998; 178: 499-503. (Medline)

4. Cunningham MJ, Dunton CJ, Com B et al. Extended field radiation therapy in early stage cervical-carcinoma: survival and complications. Gynecol Oncol 1991; 43: 51-54. (Medline)

5. Dargent D. A new future for Schauta's operation through the pre-surgical retroperitoneal pelviscopy. Eur J Gynecol Oncol 1987; 8: 292- .

6. Dargent D, Martin X, Sacchetoni A, Mathevet P. Laparoscopic vaginal radical trachelectomy: a treatment to preserve the fertility of cervical carcinoma patients .Cancer. 2000;88:1877-82. (Medline)

7. Dargent D, Ansquer Y, Mathevet P. Technical development and results of left extraperitoneal laparoscopic paraaortic lymphadenectomy for cervical cancer. Gynecol Oncol. 2000 ;77:87-92. (Medline)

8. Dargent D, Martin X, Mathevet P. Laparoscopic Assessment of the Sentinel Lymph Node in Early Cervical Cancer. Gynecol. Oncol. 2000; 79: 411-415. (Medline)

9. Dargent D. Radical trachelectomy: an operation that preserves the fertility of young women with invasive cervical cancer. Bull Acad Natl Med 2001;185:1295-304; discussion 1305-6. French. (Medline)

10. Grigsby P.W, Dehdashti F. et al. FDG-PET Evaluation of carcinoma of the cervix.In: Clinical Positron Imaging 1999; vol 2, No 2, 105-109.

11. Heller PB, Malfetano JH, Bundy BN et al. Clinical-pathologic study of stage IIB, III and IVA carcinoma of the cervix: extended diagnostic evaluation for paraaortic node metastases – A gynecologic Oncology Group study. Gynecol Oncol 1980; 38: 425-430 (Medline)

12. Holcomb K, Abulafia O, Matthews RP et al. The impact of pretreatment staging laparotomy on survival in locally advanced cervical carcinoma. Eur J Gynecol Oncol 1999; 20: 90-93. (Medline)

13. Lagasse LD, Creasman WT, Shingleton HM,et al. Results and complications of operative staging in cervical cancer. Gynecol Oncol 1980; 9; 90-98. (Medline)

14. Landoni F, Maneo A, Colombo A et al. Randomized study of radical surgery versus radiotherapy for stage Ib-IIa cervical cancer. Lancet 1997; 330: 535-440. (Medline)

15. Lanvin D, Elhage A, Henry B, et al. Accuracy and safety of laparoscopic lymphadenectomy: an experimental prospective randomized study. Gynecol Oncol 1997; 67: 83-87. (Medline)

16. Leblanc E, Caty A, Dargent D, et al. Laparoscopic lumbo-aortic lymphadenectomy in early-stage non-seminomatous germ cell tumors of the testis: Why? How? Prog Urol. 2000 ;10:379-387. French. (Medline)

17. Leblanc E, Querleu D, Narducci F, et al. Surgical staging of early invasive epithelial ovarian tumors. Semin Surg Oncol. 2000 ;19:36-41. Review. (Medline)

18. Michel G, Morice P, Castaigne D, et al. Lymphatic drainage in stage IB and II cervical cancers: anatomical study and surgical deductions] Contracept Fertil Sex 1998;26:suppl VII-XI. French. (Medline)

19. Nelson JH. Pretreatment laparotomy in stage IIB and III carcinoma of the cervix. Presented at the 1st Annual Meeting Society of Gynecologic Oncologists. January 1970

20. Nelson JH, Boyce J, Macasaet M, et al. The incidence, significance and follow-up of paraaortic lymph node metastases in late invasive carcinoma of the cervix. Am J Obstet Gynecol 1977; 128: 336-340. (Medline)

21. Querleu D, Leblanc E, Castellani B. Laparoscopic pelvic lymphadenectomy. Am J Obstet Gynecol 1991; 164: 579-581. (Medline)

22. Querleu D. Laparoscopic paraaortic node sampling in gynecologic oncology: a preliminary experience. Gynecol Oncol 1993; 49: 24-29. (Medline)

23. Querleu D, Dargent D, Ansquer Y, et al. Extraperitoneal endosurgical aortic and common iliac dissection in the staging of bulky or advanced cervical carcinomas. Cancer. 2000 ;88:1883-1891. (Medline)

24. Rose PG, Adler LP, Rodriguez M, et al. Positron emission tomography for evaluating paraortic nodal metastases in locally advanced cervical cancer before surgical staging: a surgicopathologic study. J Clin Oncol 1999; 17: 41-45. (Medline)

25. Salvat J, Schmidt MH, Vincent-Genod A, et al. Biomarkers and uterine cervical cancer. Are they useful for prognosis of cancer and triage of precancerous lesions? Contracept Fertil Sex. 1999;27:521-31. Review. French. (Medline)

26. Scheidler J, Hricak H, Yu KK, et al. Radiological evaluation of lymph node metastases in patients with cervical cancer. A meta Analysis. JAMA 1997;278: 1096-1101. (Medline)

27. Weiser EB, Bundy BN,Hoskins WJ et al. Extraperitoneal versus transperitoneal selective paraortic lymphadenectomy in the pretreatment surgical staging of advanced carvical carcinoma ( GOG study). Gynecol Oncol 1989; 33: 283-289. (Medline)