Gynecologic Oncology 93 (2004) 189 – 193 www.elsevier.com/locate/ygyno
Laparoscopic extraperitoneal paraaortic lymphadenectomy: a study of its applications in gynecological malignancies G. Mehra, a A.R.L. Weekes, b I.J. Jacobs, c D. Visvanathan, d U. Menon, c and A.R. Jeyarajah c,* a b
Clinical Research, Gynecological Oncology Unit, Barking, Havering and Redbridge NHS Trust and St. Bartholomew’s Hospital, London, UK Gynecological Oncology Unit, Barking, Havering and Redbridge Hospitals, Harroldwood, Essex and The BUPA Roding Hospital, London, UK c Department of Gynecological Oncology, St. Bartholomew’s Hospital, London EC1A7BE, UK d Gynecological Oncology Unit, Barking, Havering and Redbridge Hospitals, Essex, UK Received 16 September 2003
Abstract Objective. To describe our experience of laparoscopic extraperitoneal paraaortic lymphadenectomy and to study the feasibility, safety and applications of this technique in managing cervical, ovarian and endometrial carcinomas. Methods. Our study included 32 women with cervical, ovarian or endometrial cancers undergoing laparoscopic extraperitoneal paraaortic lymphadenectomy between December 1997 and May 2002. The operating time, nodal yield, hospital stay and complications were recorded prospectively. The impact on the overall management was assessed by comparing the preoperative therapeutic plan with that following surgicopathological staging. Results. The median nodal yield was 12 nodes, median-operating time was 80 min and the median hospital stay was 2 days. The median follow-up was 15.25 months. Lymphadenectomy was successful in all but one woman who had a peritoneal tear causing CO2 gas leakage. Complications included one case each of pulmonary embolism, umbilical hernia, lymphocoele, pelvic collection and left-thigh cellulitis. In all women, the need for adjuvant chemotherapy or extended field radiotherapy (EFRT) was based on nodal histology. The primary plan of management was changed in 22.6% women. In the endometrial and cervical cancer group, 8.3% women deferred and 20.8% additionally received EFRT. All women with ovarian cancer (stage I) were completely staged and avoided chemotherapy. Conclusion. Laparoscopic extraperitoneal paraaortic lymphadenectomy is feasible with minimal complications, acceptable nodal yield and short hospital stay. It accurately identifies those cervical and endometrial cancers requiring extended field irradiation as part of their adjuvant therapy. It can be effectively applied in staging early ovarian cancers to determine the need for adjuvant chemotherapy. D 2004 Published by Elsevier Inc. Keywords: Extraperitoneal; Paraaortic; Lymphadenectomy; Radiotherapy; Chemotherapy
Introduction Laparoscopic extraperitoneal paraaortic lymphadenectomy was first described by Vasilev and McGonigle [1] in 1996. Following this, there have been reports describing the technique and its feasibility [2– 5]. There has been a resurgence in the extraperitoneal route for lymphadenectomy based on the presumed benefits of this approach in terms of reduction in the risk of postoperative adhe* Corresponding author. Department of Gynecological Oncology, Women’s Health, King George’s V Block, 2nd Floor, St. Bartholomew’s Hospital, London EC1A7BE, UK. Fax: +44-2076017182. E-mail address:
[email protected] (A.R. Jeyarajah). 0090-8258/$ - see front matter D 2004 Published by Elsevier Inc. doi:10.1016/j.ygyno.2003.12.035
sions. The laparoscopic route itself is associated with a quick recovery and a shorter hospital stay without compromising the lymph node yield or increasing morbidity [3 –5]. In cervical cancers, the incidence of paraaortic lymph node metastasis is 6% in stage Ib, 12 –19% in stage II, 29– 33% in stage III and 30 – 40% in stage IV disease [6]. Locally advanced cervical cancer (stage z IIa) is in general treated with chemoradiation limited to the pelvis. Extended field radiotherapy (EFRT) is only undertaken if there is radiological evidence of paraaortic involvement. Extended field radiotherapy can be associated with significant gastrointestinal tract and other morbidity [7,8]. Currently available cross-sectional imaging modalities are associated with relatively poor sensitivity and specificity [9 –12]. Laparoscopic
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extraperitoneal paraaortic lymphadenectomy affords a means of detecting micrometastasis in the paraaortic nodes, thus enabling the precise selection of patients for extended field radiotherapy. Micrometastasis to lymph nodes is not recognised by cross-sectional imaging and these women would otherwise be undertreated [10]. Ovarian cancer that is apparently confined to the ovaries is associated with an excellent prognosis even in the absence of adjuvant chemotherapy [13]. In such cases, it is essential that thorough staging with lymphadenectomy, omentectomy, peritoneal cytology and biopsies are performed before making decisions regarding the use of chemotherapy. Given that metastases may disseminate directly along the gonadal vessels to the paraaortic area, the laparoscopic extraperitoneal approach may be an invaluable tool in the precise staging of apparently early disease. Involvement of the extraperitoneal lymph nodes would upstage the disease to FIGO stage IIIc with important prognostic and therapeutic implications. In women with endometrial cancers, the advantage of lymphadenectomy includes accurate staging and determination of prognosis [14]. In practise, the extent of lymphadenectomy in stages I and II disease varies from periaortic and selective pelvic node sampling to pelvic lymph node clearance or no lymph node dissection at all. Although, the role of lymphadenectomy still remains contentious, it is likely to reduce the need for radiotherapy and have a possible benefit from lymph node ‘debulking’ [15]. The histological assessment of the paraaortic nodes, especially in cancers of high grade or those with radiological evidence of paraaortic nodal disease, helps to accurately select the candidates for extended field radiotherapy. In this paper, we describe our experience of this technique and demonstrate its applications in the management of gynecological cancers.
Operative technique The procedure was carried out in the supine position. An initial transperitoneal inspection of the peritoneal cavity was undertaken in all women after obtaining a pneumoperitoneum with Verres needle inserted in the left subcostal region at Palmer’s point (3 cm below the subcostal margin in the midclavicular line) followed by a 5-mm trocar insertion for the laparoscope at the umbilicus. In ovarian cancer patients who had not had complete staging at their initial procedure, omentectomy, peritoneal biopsies and peritoneal washings were initially carried out transperitoneally. A 3-cm incision was made at the left MacBurney’s point, 3 cm medial to the left anterior superior iliac spine. Skin and underlying subcutaneous fat and fascia were incised and the muscle layers separated. Blunt finger dissection was used to create an extraperitoneal space under the control of transperitoneal laparoscopy taking care to preserve the peritoneum. Dissection was first carried out to the anterior surface of the psoas muscle and then directed cranially along the psoas muscle to the level of iliac crest and then laterally. A 10-mm trocar was then inserted at this incision and the extraperitoneal space insufflated with CO2 while exsufflating the peritoneal cavity at the same time. A second 5-mm trocar was introduced in the mid-axillary line in the extraperitoneal space 5 cm below and lateral to the first one. A third trocar of 10-mm size was then inserted 5 cm above this trocar. Further dissection in the extraperitoneal space was carried out using grasping forceps through these trocars. The peritoneum was released from the left psoas muscle medially to identify the left gonadal vessel and the left ureter, the latter being retracted with the peritoneum. The common iliac vessels along with the aorta were identified and the dissection was continued cranially till the renal vein. Bilateral paraaortic, presacral and precaval lymph node groups were excised by a combination of blunt and sharp dissection. Bipolar diathermy was used to achieve haemostasis.
Methods Data was collected prospectively from all women who underwent laparoscopic extraperitoneal paraaortic lymphadenectomy for various gynecological malignancies at the joint cancer centres of St. Bartholomew’s Hospital (London) and The Barking, Havering and Redbridge Hospitals Trust (Essex) and The BUPA Roding Hospital (London), United Kingdom from December 1997 to May 2002. Lymph nodes were said to be enlarged on MRI or CT scan if they measured more than 1 cm in their maximum short axis diameter. The assessment of the paraaortic nodes by cross-sectional imaging was compared with the histology of the nodes. The total yield of paraaortic lymph nodes was determined by histology. Operative time was calculated from the first incision to completion of surgery using anaesthetic charts. Each woman was followed up till May 2002 recording both the early and late complications.
Results and discussion Our experience Laparoscopic paraaortic lymphadenectomy was performed in 32 women for cervical, ovarian and endometrial malignancies over a period of 4 years and 5 months. Table 1 illustrates the patient characteristics of the women undergoing surgery and the types of tumours. There were two FIGO stage Ib1 cervical cancer cases with bulky disease. The paraaortic nodes were positive on histology for one woman but negative for the other. In the ovarian cancer group, one woman had recurrent carcinoma after 6 years following treatment for stage Ia disease while the other six women were referred to our unit having been diagnosed with primary ovarian carcinoma following surgery for an adnexal mass. Amongst the two women who had endometrial
G. Mehra et al. / Gynecologic Oncology 93 (2004) 189–193 Table 1 Patient characteristics and FIGO stage of carcinoma Total number of women (N) Median Age (years)
32 58.5; (30 – 82) 2; (0 – 9)
Parity (median) Site of carcinoma Cervical (n = 23)
FIGO Stage Histological Types Stage Ib1 2 squamous cell Stage Ib2 3 adenocarcinoma Stage IIa 3 endometroid Stage IIb 11 clear cell Stage IIIb 1 Stage IVa 3 Ovarian (n = 7) Stage Ia 5 endometroid Stage Ic 1 clear cell mesonephroid Recurrent 1 serous cystadenocarcinoma Endometrial (n = 2) Stg Ia grI 1 adenocarcinoma Stg Ic grIII 1 clear cell mesonephroid
15 4 3 1
5 1 1 1 1
carcinoma (stage I), one had apparent paraaortic nodal involvement on MRI, while the other had a high-grade tumour. The operative time, paraaortic lymph node yield and hospital stay are shown in Table 2. The median operative time in our series is a slight overestimation of the actual time taken to perform a laparoscopic paraaortic lymphadenectomy as 58.4% of our women had additional surgical procedures (Table 3). These included 11 pelvic lymph node dissections and three cases each of omentectomy and oophorectomy. Two cases each of adhesiolysis, vaginal hysterectomy and cystoscopy were performed while there was one case each of laparoscopic-assisted vaginal hysterectomy, pelvic mass excision, bladder biopsy and dilation and curettage, respectively. While Vergote et al. [5] had a median duration of 64 min and restricted the extent of dissection up to the superior mesenteric artery, Dargent et al. [2] had a similar increase in the operative time when the lymphadenectomy was extended till the left renal vein. The nodal yield with left-sided laparoscopic extraperitoneal paraaortic lymphadenectomy is encouraging. In our series, we had a median nodal yield of 12 paraaortic nodes (range 5 –22 nodes). Other series adopting the same route had a similar yield of nodes ranging from 6 to 20 nodes [2 – 5]. We adopt the left-sided extraperitoneal approach based on the evidence that this approach is not only comparable to the bilateral extraperitoneal approach in terms of nodal yield but also has a shorter operative time [2]. Furthermore, the adequacy of nodal clearance when compared to other approaches has also been demonstrated [2,16,17].
Table 2 Nodal yield, operating time and hospital stay Paraaortic nodal yield Operating time (min) Hospital stay (days)
12 (median); 5 – 22 (range) 80 (median); 40 – 200 (range) 2 (median); 1 – 5 (range)
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Table 3 Additional procedure with laparoscopic extraperitoneal paraaortic lymphadenectomy Pelvic lymphadenectomy Omentectomy Oophorectomy Adhesiolysis Vaginal hysterectomy Cystoscopy LAVH Pelvic mass excision Bladder biopsy Dilation and curettage Total number
11 3 3 2 2 2 1 1 1 1 17
The median hospital stay was 2 days in our series. Vergote et al. [5] had even a shorter period of hospital stay in majority of their cases in whom they solely performed paraaortic lymphadenectomy. Three women in our series had a prolonged hospital stay for 5 days. The first developed acute bronchospasm following extubation and required admission to the intensive care unit. The second had postoperative diarrhoea with abdominal discomfort, while the third required prolonged opioid analgesia. Although none of our women had conversion to laparotomy during surgery, the duration of hospital stay was influenced by those who waited for assessment by the multidisciplinary team for planning further management. Paraaortic lymphadenectomy was successfully carried out in 31 women. Surgery was abandoned in one woman when there was gas leaking into the peritoneal cavity through a tear in the peritoneum preventing development of the extraperitoneal space. She had cervical carcinoma (FIGO stage IIb) and subsequently received pelvic chemoradiation. Failure to obtain extraperitoneal insufflation can be one of the technical problems faced with the laparoscopic extraperitoneal route. Similar experiences have been quoted by others [2,5]. Vergote et al [5] had five peritoneal tears, while Dargent et al [2] had three peritoneal tears in their series of 21 cases each. We encountered two major complications (Table 4). One woman presented 7 days after surgery with an umbilical hernia through the port site and underwent an exploratory laparotomy. Another woman developed pulmonary emboTable 4 Complications of laparoscopic extraperitoneal paraaortic lymphadenectomy Early complications Minor complications Postoperative pain (prolonged analgesia) Postoperative urinary retention Diarrhoea Major complications Pulmonary embolism Umbilical hernia Late complications Pelvic collection Lymphocoele Cellulitis of left thigh
1 1 1 1 1 1 1 1
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lism requiring anticoagulation. The late complications included a lymphocoele presenting 6 months following surgery, which was managed conservatively. It has been speculated that the risk of lymphocoele is higher with extraperitoneal route probably due to the relative lack of a lymphatic network when compared with the peritoneal cavity [18]. However, this risk is low and the drainage of lymph may be facilitated by making holes in the peritoneum at the end of the procedure. The rate of lymphocoele in our series was 3.2%. One woman who developed a pelvic abscess underwent aspiration under ultrasound guidance while the other who presented with cellulitis in the left thigh was successfully treated with antibiotics. There were no injuries to major vessels in our series. Management applications Information on the histology of paraaortic nodes led to a management decision for all women who had their surgery carried out successfully. In the endometrial and cervical cancer group, the final decision for extending the field of radiotherapy to the paraaortic area was made when histology of paraaortic nodes confirmed nodal metastasis. In the ovarian cancer group, chemotherapy was indicated when paraaortic nodes were involved. In the whole group, eight women had metastatic paraaortic nodes on histology. Amongst the 31 women completing surgery, 22.6% women had their original management plan changed following histological diagnosis after paraaortic lymphadenectomy. In our series, 27 women had preoperative assessment of paraaortic nodes with either MRI or CT scan (Table 5). The overall accuracy of our cross-sectional imaging was 70.4%. Amongst the ovarian cancer group which was composed of one recurrent cancer and six primary cancers referred to the cancer unit, the woman with the recurrence had positive nodes on histology despite normal assessment by CT scan. She appropriately received adjuvant chemotherapy. Amongst the other six women who had been apparently staged as FIGO stage I following surgery for an adnexal mass, four had undergone a total abdominal hysterectomy with bilateral salpingo-oophorectomy while the other two had had oophorectomy as the primary procedure. All six women underwent laparoscopic extraperitoneal paraaortic lymphadenectomy as part of their final staging. All were confirmed to have stage I disease on histology with no nodal involvement. Paraaortic lymph node metastasis may be present in as many as 30% of women with apparent early stage ovarian carcinoma [13]. The histological assessment of paraaortic nodes in early stage disease helps to separate women with nodal disease requiring chemotherapy from those without any nodal involvement and a good prognosis with surgery alone. The correct stage and the treatment with adjuvant therapy can be decided accurately following laparoscopic extraperitoneal paraaortic lymphadenectomy. In the cervical and endometrial cancer group, our study demonstrates the significance of histological diagnosis of
Table 5 Paraaortic nodal assessment by MRI or CT scan (n = 27)
Positive nodes on MRI/CT Negative nodes on MRI/CT
Positive histology
Negative histology
2 6
2 17
paraaortic nodal involvement and how this is feasible with laparoscopic extraperitoneal approach. At present, the routine assessment of the paraaortic nodes rely on crosssectional imaging and, both MRI and CT scan, have their own limitations with the overall sensitivity ranging from 38% to 75% [10 – 12]. In this group, a preoperative assessment of the paraaortic nodes was done in 23 women. If only paraaortic nodal assessment by MRI or CT scan would have been considered in this group, 20.8% of women with paraaortic nodal metastasis would have failed to receive treatment with extended field radiotherapy while 8.3% women would be unnecessarily irradiated. Although, there is no evidence that extended field radiotherapy offers any survival benefit in cervical cancer, it is the preferred means of treating women with metastatic disease in the paraaortic nodes [19,20]. The accurate assessment by laparoscopic extraperitoneal lymphadenectomy allows us to treat women appropriately as it not only helps to avoid the relatively high morbidity associated with extended field radiotherapy, but also accurately identifies those women who might benefit from it.
Conclusion Left-sided laparoscopic extraperitoneal paraaortic lymphadenectomy is a safe procedure with an acceptable nodal yield, complication rate and a short hospital stay. It is effective in tailoring the field of adjuvant radiotherapy in cervical and endometrial cancers allowing precise treatment. It is useful as a tool for completing staging and confirming adequate treatment in early stage ovarian cancers. References [1] Vasilev SA, McGonigle KF. Extraperitoneal laparoscopic para-aortic lymphnode dissection. Gynecol Oncol 1996;61:315 – 20. [2] Dargent D, Ansquer Y, Mathevet P. Technical development and results of left extraperitoneal laparoscopic paraaortic lymphadenectomy for cervical cancer. Gynecol Oncol 2000;77(1):87 – 92. [3] Querleu D, Dargent D, Ansquer Y, Leblanc E, Narducci F. Extraperitoneal endosurgical aortic and common iliac dissection in the staging of bulky or advanced cervical carcinomas. Cancer 2000; 88(8):1883 – 91. [4] Schlaerth JB, Spirtos NM, Carson LF, Boike G, Adamec T, Stonebraker B. Laparoscopic extraperitoneal lymphadenectomy followed by immediate laparotomy in women with cervical cancer: a gynecologic oncology group study. Gynecol Oncol 2002;85(1):81 – 8. [5] Vergote I, Amant F, Berteloot P, Gramberen MV. Laparoscopic lower para-aortic staging lymphadenectomy in stage IB2, II and III cervical cancer. Int J Gynecol Cancer 2002;12:22 – 6.
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