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10.1245/ASO.2004.07.005
Annals of Surgical Oncology 11:344-349 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Laparoscopic Sentinel Node Procedure Using a Combination of Patent Blue and Radiocolloid in Women With Endometrial Cancer

Emmanuel Barranger, MD, Annie Cortez, MD, Dany Grahek, MD, Patrice Callard, MD, PhD, Serge Uzan, MD and Emile Darai, MD, PhD

From the Departments of Gynecologic and Breast Cancers (EB, SU, ED), Pathology (AC, PC), and Nuclear Medicine (DG), Hôpital Tenon, Assistance Publique des Hôpitaux de Paris, Paris, France.

Correspondence: Address correspondence and reprint requests to: Emmanuel Barranger, MD, Department of Gynecologic and Breast Cancers, Hôpital Tenon, 4 rue de la Chine, 75020 Paris, France; Fax: 33-1-56-01-60-62; E-mail: emmanuel.barranger{at}tnn.ap-hop-paris.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We assessed the feasibility of a laparoscopic sentinel node (SN) procedure based on the combined use of radiocolloid and patent blue labeling in patients with endometrial cancer.

Methods: Seventeen patients (median age, 69 years) with endometrial cancer of stage I (16 patients) or stage II (1 patient) underwent a laparoscopic SN procedure based on combined radiocolloid and patent blue injected pericervically. After the SN procedure, all patients underwent complete laparoscopic pelvic lymphadenectomy and either laparoscopically assisted vaginal hysterectomy (16 patients) or laparoscopic radical hysterectomy (1 patient).

Results: SNs (mean number per patient, 2.6; range, 1–4) were identified in 16 (94.1%) of the 17 patients. Macrometastases were detected in three SNs from two patients by hematoxylin and eosin staining. In three other patients, immunohistochemical analysis identified six micrometastatic SNs and one SN containing isolated tumor cells. No false-negative SN results were observed.

Conclusions: An SN procedure based on a combination of radiocolloid and patent blue is feasible in patients with early endometrial cancer. Combined use of laparoscopy and this SN procedure permits minimally invasive management of endometrial cancer.

Key Words: Sentinel node • Laparoscopy • Patent blue • Radiocolloid • Endometrial cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Endometrial carcinoma is the most frequent gynecological malignancy in industrialized countries. In the United States, 36,000 new cases of endometrial cancer and 6,400 deaths were reported in 2000.1 In Europe, 4,600 new cases of endometrial cancer were diagnosed in 1995, corresponding to a standardized incidence rate of 13.6 cases per 100,000 women. In France, endometrial cancer was responsible for 1200 deaths in 1995, making it the third most frequent female malignancy (after breast and colorectal cancer).

Surgical management of early-stage endometrial cancer includes peritoneal cytology, total hysterectomy with bilateral salpingo-oophorectomy, and lymph node sampling.2 Histological grade, depth of myometrial involvement, and lymph node status are the main prognostic factors in endometrial cancer.3 The International Federation of Obstetricians and Gynecologists4 recommends pelvic lymphadenectomy to assess lymph node status in this setting, whereas the Gynaecological Oncology Group recommends systematic pelvic and para-aortic lymphadenectomy. However, the latter approach is associated with significant morbidity. Moreover, the proportion of women who have pelvic lymph node involvement ranges from 4.7% to 13% and from 18.8% to 44.8% in stage I and stage II endometrial cancer, respectively.5–10 Thus, approximately 8 in 10 women with stage I endometrial cancer derive no benefit from lymphadenectomy; worse, this procedure may be associated with additional morbidity, particularly when postoperative radiotherapy is required.11,12

The sentinel node (SN) procedure is increasingly used as an alternative to systematic lymphadenectomy, with the aims of avoiding excess morbidity and improving lymph node staging while at the same time preserving control of regional disease. The term sentinel node—the first lymph node encountered by lymphatic vessels draining a tumor—was coined in 1960 by Gould et al.13 for cancer of the parotid gland. The SN procedure has since been validated in vulvar cancer14–16 and is being assessed in cervical cancer.17–23 In contrast, few studies have examined use of the SN procedure in endometrial cancer.24–27 The aim of this prospective study was to evaluate the feasibility of a laparoscopic SN procedure based on a combination of radiocolloid and patent blue labeling in women with endometrial cancer.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From July 2002 to May 2003, 17 consecutive patients with endometrial cancer were included in this prospective study. The inclusion criteria were biopsy-confirmed endometrial cancer of clinical stage I or II according to the criteria of the International Federation of Gynecology and Obstetrics.2 All the patients underwent preoperative blood sampling, chest radiography, hysteroscopy, and pelvic magnetic resonance imaging.

Patients with stage I disease underwent laparoscopic treatment, including peritoneal washing, bilateral salpingo-oophorectomy, the SN procedure, systematic pelvic lymphadenectomy, and laparoscopically assisted vaginal hysterectomy. Patients with stage II disease underwent a peritoneal washing, bilateral salpingo-oophorectomy, and the SN procedure, followed by systematic pelvic lymphadenectomy and laparoscopic radical hysterectomy. In accordance with the French National Federation of Cancer28 and the International Federation of Gynecology and Obstetrics,4 no systematic para-aortic lymphadenectomy was performed. However, in accordance with our institutional protocol, para-aortic lymphadenectomy was performed when a para-aortic SN was detected or when positive SNs were found by intraoperative histological examination.

Our institutional review board approved the protocol. All patients gave their written consent after receiving relevant information, including the potential adverse effects of patent blue, radiocolloid, general anesthesia, and laparoscopy and the possible need to convert to open surgery.

SN Procedure
Four pericervical injections (1.5-cm depth) of .2 mL (10 MBq each) of unfiltered 99mTc sulfur colloid (Nanocis; CIS Bio International, Saclay, France) were administered with a 25-gauge spinal needle on the day before surgery. Scintigraphic images were obtained 2 hours after the injections and then every 30 minutes until the SN was visualized, by using a triple-head gamma camera (Irix; Marconi Corp., Cleveland, OH). Five-minute static anterior projection was acquired with a low-energy/high-resolution collimator and a matrix size of 256 x 256 pixels. When the SN was not visualized on the day of the injection, imaging was repeated the next day, 2 hours before surgery.

The patients were placed, under general anesthesia, in a low lithotomy position. A speculum was placed in the vagina, and patent blue (Bleu Patenté V; Guerbet Laboratory, Issy les Moulineaux, France) was injected pericervically (1 mL per injection; 1.5 cm deep) with a 25-gauge spinal needle at 3 and 9 o’clock. Antimicrobial chemoprophylaxis (cefazolin 2 g intravenously) was administered at the beginning of the operation. Subcutaneous heparin prophylaxis was started the day before surgery and was continued for 10 days. In laparoscopic procedures, after pneumoperitoneal insufflation with a Veress needle, a 10-mm laparoscope was inserted through an umbilical incision and connected to a video monitor. Three stab incisions were made in the suprapubic region: one 12-mm incision in the midline (Versaport; Auto Suture Co., Elancourt, France) and one 5.5-mm incision in each iliac fossa.

After patent blue injection, the pelvic and lower para-aortic regions were carefully inspected for lymph ducts and specific dye uptake by lymph nodes. "Hot" pelvic and para-aortic nodes were located by using an endoscopic gamma probe (Eurorad, Strasbourg, France) inserted through the 12-mm suprapubic trocar. Hot nodes were detected before the peritoneum was opened. The gamma probe was angled laterally to avoid detection of residual radioactivity at the injection site.

After location of the SN, the peritoneum was opened above the external iliac vessels to the round ligament. Each blue or hot node was removed separately in an endoscopic bag (Endocatch; Auto Suture Co.). The position of each SN relative to the major pelvic vessels and the count rate were recorded.

Laparoscopic bilateral pelvic lymphadenectomy was performed systematically after the SN procedure. All node tissue along the obturator fossa and the external vessels, up to the iliac bifurcation, was extracted in an endoscopic bag. The absence of residual pelvic or para-aortic radioactivity was verified before laparoscopically assisted vaginal hysterectomy or laparoscopic radical hysterectomy.

The duration of the laparoscopic procedure was calculated from the insertion of the Veress needle to the last skin suture. The duration of the SN procedure was calculated from the insertion of the endoscope to the extraction of the last SN from the abdomen.

Histopathologic Evaluation
A pathologist inspected SNs and other pelvic nodes. Grossly metastatic nodes were sectioned. Normal-appearing SNs were cut perpendicular to the long axis. All SNs were examined during surgery by imprint cytology. Air-dried cytological smears were prepared by scraping the cut surfaces and were stained with a rapid May-Grünwald-Giemsa method. Each half-SN was sectioned at 3-mm intervals. Each 3-mm section was analyzed by four additional levels of 150 µm and four parallel sections; one section was used for hematoxylin and eosin (H&E) staining, and H&E-negative sections were then examined by immunohistochemistry (IHC) with an anticytokeratin antibody cocktail (cytokeratin AE1–AE3; Dako Corp., Glostrup, Denmark). Non-SNs were totally submitted and blocked individually following 3-mm distances and H&E staining.

The size of nodal metastases was estimated with an eyepiece micrometer. Micrometastasis was defined as a single focus of metastatic disease measuring no more than 2 mm in a given node. The presence of single noncohesive tumor cells was recorded. SNs were considered positive for tumor involvement when they contained macrometastases, micrometastases, or isolated tumor cells.

Analysis
SNs were recorded as blue-stained or hot (i.e., the ex vivo count exceeded three times the background radioactivity). The false-negative rate was defined as the number of procedures with a negative SN and one or more positive non-SNs divided by the number of procedures with any positive pelvic lymph nodes.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Characteristics
The 17 patients’ demographic data and tumor characteristics are shown in Table 1. The median age was 69 years (range, 46–79 years). The median body mass index was 24.2 kg/m2 (range, 17.4–33.4 kg/m2). All the patients were postmenopausal, and four were receiving hormone-replacement therapy. Fourteen patients had endometrioid adenocarcinoma, two patients had papillary serous carcinoma, and one patient had a malignant mixed Müllerian tumor. All SN procedures used both radiocolloid and patent blue. None of the patients had magnetic resonance imaging evidence of lymph node involvement.


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  		TABLE 1. Patient demographics and tumor characteristics
 
Lymphoscintigraphy
Lymphoscintigraphy was always performed the day before surgery and showed one focus or several uptake foci corresponding to SNs in 16 of the 17 patients. Thirteen patients had bilateral hot SNs. Except for one SN that was located in the aortic bifurcation, all SNs were found in the pelvis. All patients found the radiocolloid injections painful, but none requested analgesics.

Laparoscopic SN Procedure
The median interval between patent blue injection and the beginning of the laparoscopic SN procedure was 6 minutes (range, 5–10 minutes). The median duration of the laparoscopic SN procedure was 17 minutes (range, 10–30 minutes).

SNs were identified in 16 patients (94.1%). The patient in whom no SNs were identified by lymphoscintigraphy had no blue or hot SNs detected by laparoscopy. The mean number of SNs was 2.6 per patient (range, 1–4). A total of 42 SNs were removed. Of these, 39 were both blue and hot, and 3 were only hot; none was only blue.

Ten patients had bilateral SNs, and six patients had a unilateral SN (right and left side in three cases each). The most common site of the SNs was the medial external iliac region (50%; Table 2). No SNs were found in the parametrium. The patient with an SN in the aortic bifurcation also had two external iliac SNs.


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  		TABLE 2. Location of the 42 sentinel lymph nodes (SNs)
 
The median number of removed lymph nodes was 11 per patient (range, 4–15). None of the 17 patients required para-aortic lymphadenectomy, because no para-aortic SNs were detected and no positive SNs were found by intraoperative histological examination.

The median total operating time, including the laparoscopic SN procedure, complete node tissue removal, bilateral salpingo-oophorectomy, and hysterectomy, was 150 minutes (range, 120–280 minutes). No anaphylactic reactions to patent blue occurred. No complications occurred during thelaparoscopic SN procedure, and laparoconversion was never necessary.


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  		TABLE 3. Sentinel node procedures in endometrial cancer: a review of the literature
 
Histological Findings
None of the 42 SNs showed signs of malignancy on intraoperative imprint cytology. Ten SNs (23.8%) from five patients (31.3%) were found to be metastatic at the final histological assessment. Of these five patients, two had grade 1, one had grade 2, and two had grade 3 endometrial cancer. All positive SNs were both blue and hot.

Among the 10 positive SNs, H&E staining revealed macrometastases in 3 SNs from 2 patients. These three SNs (both blue and hot) were all located in the medial external iliac region. One of these two patients with stage I endometrial cancer had a macrometastatic SN and a positive ipsilateral pelvic node.

IHC analysis revealed micrometastases in six SNs and isolated tumor cells in one SN (three patients). Four of the six micrometastatic SNs were located in the interiliac area, one was in the obturator fossa, and one was in the medial external iliac region. All non-SNs were negative. No false-negative SN results were obtained.

Patients with metastatic SNs detected by H&E or metastatic pelvic non-SNs underwent postoperative pelvic irradiation and chemotherapy. No chemoradiotherapy was prescribed for women with micrometastases or isolated tumor cells detected by IHC.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study demonstrates the feasibility of a laparoscopic SN procedure based on combined labeling with radiocolloid and patent blue in patients with early-stage endometrial cancer. We detected SNs in 16 (94.1%) of 17 patients. These results are partly in contrast with previous studies on the SN procedure in patients with endometrial cancer (Table 3). In a study of 15 patients with endometrial cancer, Burke et al.24 reported an SN detection rate of 67% with a laparotomic procedure based on blue dye alone. In a preliminary study of eight patients, Echt et al.,25 also using blue dye alone, detected no SN. In contrast, Holub et al.,26 using a laparoscopic SN procedure with blue dye alone in 25 patients, identified SNs in 72% of cases. Our high identification rate of SNs underlined that the SN procedure with combined detection is the most appropriate technique for SN detection. Indeed, Pelosi et al.,27 using a combined detection method, also reported a high identification rate of SNs (SNs were detected in all 11 patients studied).

We used pericervical injections of both patent blue and radiocolloid, whereas subserosal myometrial injections were also used in previous studies.24–26 The pericervical injection technique is well standardized and allows a comparison between the patent blue and radiocolloid techniques for SN detection. In contrast, myometrial injection of radiocolloid the day before surgery is technically difficult. There is no consensus on the optimal sites or number of fundal injections.24–26 Although direct para-aortic lymph node drainage of the uterine fundus has been proven by anatomical studies,29,30 the superiority of combined fundal and pericervical injections over pericervical injections alone for the detection of SNs in patients with endometrial cancer has not been demonstrated. Holub et al.26 reported an SN identification rate of 83.3% after pericervical and subserosal myometrial injections of blue dye, compared with 61.5% after subserosal myometrial injections alone. Burke et al.24 injected blue dye into three subserosal myometrial sites and identified SNs among removed lymph nodes in only 27% of cases (four patients). In two patients, the nodal metastases were located in nodes marked by blue dye. The third patient had a negative para-aortic SN, but metastases were found in an obturator non-SN. The fourth patient had multiple pelvic metastases but no dye uptake in any lymph node. With a false-negative rate of 25%, the authors concluded that subserosal myometrial injection of patent blue was unsuitable for SN procedures. It has not yet been shown whether subserosal myometrial injection of patent blue increases the SN detection rate relative to combined pericervical injections of patent blue and radiocolloid.

In our study, all but three SNs were located in the external pelvic area, essentially in the external iliac region. SNs are less frequently located in the common iliac region, and no parametrial SN was detected (Table 4). Only one woman had an aortic bifurcation SN, which was associated with two external iliac SNs. Using subserosal myometrial injections, Burke et al.24 found para-aortic SNs in 38% of cases but did not specify whether these para-aortic SNs were associated with external or common iliac SNs. Para-aortic metastasis without pelvic lymph node involvement is found in only 1% to 2% of patients with endometrial cancer.31 Although lymphatic spread from the uterine corpus to the para-aortic area is not frequent,29,30 the data reported by Burke et al.24 raise the issue of whether fundal injection of patent blue should be added to pericervical patent blue and radiocolloid injections. Our data confirm those of Mariani et al.,32 who reported that external iliac lymph nodes were the most commonly involved lymph nodes in patients with endometrial cancer.


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  		TABLE 4. Location of sentinel lymph nodes (SN) in patients with endometrial cancer
 
Although we performed pericervical injections, a unilateral pelvic SN was found in 6 (36.5%) of 16 patients. In previous studies17,19–21 performing SN procedures by cervical injections in patients with cervical cancer, the frequency of unilateral SNs varied from 50% to 61.5%. This relatively high rate of unilateral SNs could be explained by the following facts: the lymphatic drainage from the cervix is not well established and is probably not symmetrical, and the injections performed around the cervix are not strictly identical either. Furthermore, the pathologic pattern of pelvic lymph node metastases in cervical cancer is not systematically bilateral. Indeed, Michel et al.33 showed that unilateral pelvic nodal involvement was found in 55.7% of patients with cervical cancer.

Five (31.3%) of our 17 patients had nodal metastases. This high rate of lymph node involvement is probably due to the use of multiple node sectioning and IHC staining, contrary to previous studies.24–26 As in breast cancer,34 the prognostic significance of micrometastases in endometrial cancer is controversial. However, Yabushita et al.35 showed that positive cytokeratin staining of lymph nodes containing metastases that were not identified by H&E staining was a risk factor for the recurrence of stage I endometrial cancer.

In conclusion, our results confirm the feasibility of a laparoscopic SN procedure based on combined labeling with radiocolloid and patent blue in patients with endometrial cancer. This procedure can contribute to minimally invasive management. Further studies are required to confirm that this SN procedure is a valid alternative to systematic lymphadenectomy in patients with endometrial cancer.


   FOOTNOTES
 
This study demonstrates the feasibility of a laparoscopic sentinel node procedure based on combined detection with patent blue and radiocolloid in patients with endometrial cancer.

Received for publication July 14, 2003. Accepted for publication November 13, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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