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JoVE Journal Cancer Research

Cancer Research

Sentinel Lymph Node Mapping and Biopsy for Endometrial Cancer at Early Stage with Laparoscopy

Published: August 19, 2021 doi: 10.3791/63044
Automatic Translation
1, 1, 1, 1, 1, 1
1Obstetrics and Gynecology Hospital of Fudan University

Summary

This protocol describes the identification and resection of sentinel lymph nodes to make the operation as easy and minimally invasive as possible.

Abstract

Sentinel lymph node (SLN) mapping and biopsy is a promising technique for visualizing and evaluating lymph node status in cancer. This approach has been recommended for low-risk endometrial cancer (EC) patients by authoritative international guidelines, but it has not been performed broadly in China and worldwide. This work aims to describe detailed SLN mapping and biopsy procedures to promote the clinical application. SLN mapping and postoperative pathologic ultrastaging were conducted in a patient with low-risk EC using indocyanine green (ICG) dye to track the SLNs under laparoscopy and resecting them completely for ultrastaging. In conclusion, this protocol describes details of ICG injection, and SLN mapping and biopsy in EC patients based on the experiences gained during clinical practice.

Introduction

Endometrial cancer (EC) is one of the most common diseases in gynecological oncology, and its incidence is rising1,2. Surgery is the first-line treatment for early-stage EC3,4. The evaluation of lymph node metastasis is an essential part of surgical staging in EC. The Gynecologic Oncology Group (GOG) study 33 demonstrated that lymph node metastases are associated with poor prognosis5.

As a new and essential technique for evaluating lymph node metastasis, sentinel lymph node (SLN) mapping and biopsy have emerged in recent years and have been recommended to be employed for patients with apparent uterine-confined EC according to the National Comprehensive Cancer Network (NCCN) guidelines for uterine cancer6,7,8,9,10. SLN mapping has also been extensively applied in tumors such as breast cancer11, lung cancer12, thyroid cancer13, and melanoma14. Pathologic ultrastaging has achieved good performance in colorectal and gynecological cancer15,16,17 and is recommended by the authoritative European guidelines18. Although principles of SLN mapping for EC staging have been provided in international guidelines10,19, there are no detailed manipulations of surgery in other present works.

This work presents the protocol for detailed SLN mapping and biopsy with ICG in a 28-year-old female who had been clinically diagnosed with early-stage EC, thus, improving and promoting the diagnosis of patients.

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Protocol

All surgery procedures related to the patient described here were approved by the Ethics Committees of Obstetrics & Gynecology Hospital of Fudan University in Shanghai, China. Informed consent was acquired from the patient.

1. Indications for SLN mapping with ICG in EC patients

  1. Ensure that patients are clinically diagnosed with primary EC confined to the uterus with low-risk factors (grade 1 or 2 endometrioid carcinomas, pre-surgical endometrial lesion ≤2 cm, and myometrial invasion <50%).
  2. Ensure that patients are not allergic to the developer (ICG).
  3. Ensure that patients have not experienced retroperitoneal lymph node dissection for any reason before the disease.
  4. Ensure that the patients understand the SLN surgical procedures and have signed the surgical consent forms.
  5. Ensure that the patients cannot perform systematic lymphadenectomy but SLN mapping for surgical staging for any reason.
  6. Ensure that the patients are enrolled in the clinical trial into the SLN mapping group if they are with intermediate-high risk EC.

2. Patient preparation

  1. Preoperative bowel preparation
    1. Provide laxatives for bowel preparation and enema to patients who have undergone multiple pelvic and abdomen surgeries.
      NOTE: Intestinal preparation is not required for patients without bowel surgery history.
  2. Preoperative diet preparation
    1. Avoid solid food for 8 h before the operation, prevent a semi-liquid diet for 6 h before the procedure, and stop drinking for 2 h before the procedure.
  3. Anesthesia
    1. Use intravenous agents (e.g., propofol) to produce unconsciousness and add some neuromuscular blockers by inhalation or intravenous routes to achieve the needed depth of anesthesia. Use a combination of administrations for anesthetic maintenance to ensure the patient to be unconscious and fully relaxed with stable vital signs throughout the operation.
      NOTE: The usage of anesthetics will be following the rules of the anesthesiology department of each center.
  4. Position
    1. Once the patient is anesthetized, allow the patient to be in the lithotomy position with Trendelenburg position.
  5. Prepare the skin at the surgical site. Perform skin preparation with an antiseptic preparation (e.g., povidone-iodine) in an organized fashion from the intended site of the incision radiating out to the edges of the intended area of skin exposure, with the upper boundary of flat xiphoid process, side borders of mid-axillary lines, and lower boundary of the upper thigh (Figure 1).

3. Fluorescent dye preparation

  1. Indocyanine green (ICG) preparation
    1. Dissolve 25 mg of ICG into 20 mL of sterile water for a final concentration of 1.25 mg/mL and shake gently.

4. ICG injection

  1. Use a 2 mL syringe (with the needle size of 0.6 mm x 32 mm TW LB) to inject 0.5 mL of the prepared ICG at 3 o'clock and 9 o'clock of the ectocervix at the superficial (2-3 mm) and deep (1-2 cm) cervix, respectively (Figure 2).
    ​NOTE: In some cases, the ectocervix positions of 6 and 12 o'clock can also be selected. ICG should be avoided when injected into Nessler's cyst.

5. Intraoperative SLN identification

  1. Preparation before development
    1. Grasp the skin around the umbilicus with two towel forceps to elevate the abdominal wall. Make an incision of about 10 mm wide in the skin of the umbilicus and through the fascia and peritoneum.
    2. Insert a 10 mm trocar through the umbilicus, producing the pneumoperitoneum with intraperitoneal pressure of about 13-14 mmHg. Insert a laparoscope (with light source and cameras) via the trocar.
    3. Make three other small incisions of ~5 mm wide in the lower abdomen and insert 5 mm trocars through the abdominal wall into the cavity. Insert instruments for manipulation via the other three 5 mm trocars (Figure 1).
    4. Identify the fallopian tubes under laparoscopy. Grasp and elevate the tubes close to fimbriae and tie a ligature around the tube with a 2-0/T silk suture.
      NOTE: This step is used to prevent endometrial tumor cells from entering the abdominal cavity along the fallopian tubes from the uterine cavity.
    5. Take the peritoneal washings with 100 mL of normal saline before any significant handling or manipulation of the uterus. Collect the washing fluid for cytology.
    6. Open the fluorescence mode of the endoscopic fluorescence imaging system (see step 5.2). Lift unilateral pelvic infundibulum ligament and uterus to reveal the lateral peritoneum and look for the fluorescence lymphatic vessels.
      ​NOTE: If there are no fluorescence lymphatic vessels identified, it is allowed to inject ICG repeatedly.
  2. SLN mapping
    1. Endoscopic fluorescence imaging system preparation (PINPOINT).
    2. Adjust the fluorescence mode to near-infrared laser (excitation light, 805 nm) for the best field of view.
      NOTE: The endoscopic fluorescence imaging system has several modes, such as HD (High definition) white light, SPY fluorescence, PINPOINT fluorescence, and SPY CSF mode, and the surgeon can switch to another mode if necessary.
  3. Identify SLNs under a fluorescence laparoscopy.
    1. Hold an ultrasonic scalpel and toothless forceps with each hand (performed by the surgeon).
      NOTE: The assistant grasps toothless forceps to cooperate with the surgeon.
    2. Lift and open the peritoneum, separate the sub-peritoneal fat and connective tissues to reveal the necessary structures, including the ureter, internal iliac vessels, and obturator nerves according to the indication of green fluorescence lymphatic lines, as well as to protect them from injury.
      NOTE: An ultrasonic scalpel with activation is used to cut the tissues, while an inactivated scalpel can be used for blunt dissection.
    3. Observe the SLNs covered by the peritoneum about 5-10 min after ICG injection.
      ​NOTE: Typically, SLNs present along with the fluorescence lymphatic vessels from both sides of the cervix to at least the height of the common iliac blood vessel. Occasionally, the SLNs emerge beside the abdominal aorta. PINPOINT equipment has multiple modes, including white light, fluorescence, and black and white modes. Switching between multiple modes helps to determine the location of SLNs.

6. Intraoperative SLN biopsy

  1. Locate the SLN, the first mapped lymph node along the drainage from parametrium in each hemi-pelvis, and use multiple modes to confirm it. Fully expose the SLNs for complete resection (Figure 3).
  2. Grasp and elevate the SLN by toothless forceps and perform a complete resection of the lymph node along the periphery of the lymph node in white light.
    NOTE: Avoid lymph node damage, which might cause contamination with tumor cells.
  3. Place the removed SLNs in the obturator fossa or put them into a small, simple bag. After the uterus is completely removed and taken out through the vagina, bilateral SLNs are taken out entirely through the vagina rather than through the 5 mm trocar opening to avoid fragmentation.
  4. Send the removed lymph nodes to the pathology department for pathological ultrastaging.
  5. During the operation, resect the enlarged or suspicious lymph nodes simultaneously and send them for pathological examination.
  6. Record the locations of SLNs on standardized intraoperative data collection forms.
  7. If SLN mapping fails on one or both sides, perform side-specific lymphadenectomy according to the NCCN guidelines.
    NOTE: If there is no fluorescent node in the hemipelvis, continue to seek the mapped node along the lymphatic vessels until the para-aortic region due to the possibility of mapping in unexpected locations. A failed SLN mapping on either side means that any fluorescent green node is not visible with or without fluorescent green lymphatic vessels under the fluorescence laparoscope system on either side of the pelvis and para-aortic region.
  8. Perform a total hysterectomy plus bilateral salpingectomy.
    ​NOTE: Since this was a 28-year-old patient with early-stage endometrioid cancer who had a strong desire for fertility preservation and normal-appearing ovarian cancer and had no apparent family history of breast/ovarian cancer or Lynch Syndrome, ovarian preservation could be considered.
  9. Indwell a drainage tube for potential residual fluid in the pelvis.
  10. Remove the laparoscope and release the gas from the abdomen. Close the incisions in the umbilicus and lower abdomen with a single stitch by 2-0/T silk suture.

7. Postoperative SLN ultrastaging20

  1. Cut the SLN along the maximum diameter and micro-sectioned 50 µm apart to get three hematoxylin-eosin (H&E) slides and one immunohistochemistry (IHC) slide with anti-cytokeratin antibody (AE1/AE3).
    NOTE: Ultrastaging entails thin serial sectioning of the gross SLN. Cytokeratin IHC is not essential. No standard protocol is for ultrastaging.
  2. Lymph node metastases were described as macrometastases (>2 mm), micrometastases (0.2-2.0 mm), or isolated tumor cells (ITCs) according to the classification of the American Joint Committee on Cancer (AJCC)21.
  3. Report the postoperative pathology with details about the tumor size, histologic type and grade, myometrial invasion, lymphovascular space involvement, cervical stromal involvement, number and status of per lymph nodes, and the cytology of peritoneal washings.

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Representative Results

The patient in the present case was a 28-year-old female with irregular vaginal bleeding for 2 years, and she was diagnosed with an abnormality of the endometrium 4 months ago. Transvaginal ultrasound examination revealed a heterogeneous endometrial thickness with an adnexal mass. Abdominopelvic magnetic resonance imaging (MRI) demonstrated a 51 mm x 56 mm x 88 mm mass with a clear boundary within the uterine cavity under a high T2WI signal in a local hospital. Then, she was evaluated by hysteroscopy, and the endometrial lesion was dissected. The pathological results showed grade 1 endometrial cancer. This patient came to the hospital for further treatment with a strong fertility requirement. After a comprehensive evaluation (including another MRI examination that showed an irregular signal of endometrium in hospital, Figure 4) and signing informed consent, she experienced fertility preservation treatment. However, the second hysteroscopy in the hospital revealed superficial myometrial invasion, a contraindication of fertility preservation. Ultimately, after the patient was informed of her condition, she decided to undergo a total hysterectomy + bilateral salpingectomy + SLN mapping.

The cervix was injected with diluted ICG at 3 and 9 o'clock positions superficially and deeply, respectively (Figure 2). Then, the lymphatic vessels and SLNs were fluorescently labeled, which allowed for their recognition under various color modes (green for fluorescence mode and blue and red for color-segmented mode) in the Pinpoint Endoscopic Fluorescence Imaging system (Figure 3). Subsequently, the pathology department conducted H&E and IHC staining of SLN (Figure 5 and Figure 6) and ultrastaging of SLN. The staging results revealed a negative metastasis output.

Figure 1
Figure 1: Antiseptic preparation scope of SLN mapping in EC with laparoscopy. The black arrow indicates mid-axillary lines. The numbered red circles indicate the places of four trocars on the abdominal wall. Circle No. 2 is for the 10 mm trocar. The rest of the circles are for 5 mm trocars. The distance between circles No. 2 and 3 is around four fingerbreadths. Please click here to view a larger version of this figure.

Figure 2
Figure 2: Illustration of the SLN mapping in EC. (A) Anatomical diagram of the SLN in the pelvis. The dark green line represents the direction of the lymphatic drainage. Arrows indicate SLN lymph nodes in this case (yellow arrow presents the lymph node located between the right external and internal iliac vessels, brown arrow demonstrates the SLN in the left obturator foramen, and black arrow shows enlarged lymph node on the left iliac vein). Blue flat line indicates clock directions. (B) Injection spot locations in the cervix. ICG = indocyanine green. Green dots indicate the injection spots. The blue square shows the 3 and 9 o'clock positions of the ectocervix. (C) Enlarged cervix diagram: green dots indicate superficial and deep cervical injections. Please click here to view a larger version of this figure.

Figure 3
Figure 3: Intraoperative imaging of the SLN in EC. (A) Fluorescence mode. The green arrow indicates the SLN under fluorescence mode. (B) Color-segmented fluorescence mode. The yellow arrow indicates the lymph node under color-segmented mode. (C) Florescence mode of sentinel lymph nodes of this case. (D) Color-segmented fluorescence mode of sentinel lymph nodes of this case. HD: High definition; CSF: Color-segmented fluorescence. Please click here to view a larger version of this figure.

Figure 4
Figure 4: The MRI of EC patient. (A) Irregular signal of the endometrium located in the lower uterus cavity (arrows) on T1WI. (B) Irregular signal of the endometrium (arrows) on T2WI. Please click here to view a larger version of this figure.

Figure 5
Figure 5: H&E staining of EC and IHC staining of SLN. (A) H&E staining of myoinvasion in EC. (B) H&E staining of SLN. (C) IHC staining of AE1/AE3 (AE1/AE3 may stain myofibroblasts and smooth muscle cells and indicate the residual tumor cells) in SLN. 2.5x and 5x refer to the magnification under the microscope. Please click here to view a larger version of this figure.

Figure 6
Figure 6: IHC staining of EC patients. (A) IHC staining of estrogen receptor (ER) with five magnifications. (B) IHC staining of progesterone receptor (PR). (C) IHC staining of P53. (D) IHC staining of Ki67. (E) IHC staining of MLH1. (F) IHC staining of MSH2. (G) IHC staining of PMS2. (H) IHC staining of MSH6. All the images are captured with 5x magnification. Please click here to view a larger version of this figure.

Table 1: Comparison between tracers of blue dye, ICG, and Tc99. Please click here to download this Table.

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Discussion

SLN mapping and biopsy is a more selective and tailored lymph node dissection approach that has been applied in the clinic for nearly 20 years. In the field of EC, SLN mapping and biopsy have been increasingly recommended by several guidelines due to their high diagnostic efficiency in early-stage EC, achieving overall and bilateral detection rates of 89%-95% and 52%-82%, respectively, with a sensitivity of 84%-100% and negative predictive value of 97%-100%22. The present study reports a typical EC patient who performed SLN mapping and described the SLN protocol in detail from ICG injection to SLN biopsy.

SLN mapping is feasible with various dyes. Previous research on lymph node staging of breast and endometrial cancers applied blue dye (usually methylene blue or isosulfane blue (ISB), radiocolloid, or both23,24,25,26), reaching good performance and accuracy. As shown in white light, the blue dyes mentioned above have been extensively used due to their convenience and the least complex equipment requirement. However, the ICG dye had higher SLN detection rates (83%) than the ISB (64%)26. Thus, ICG is considered a better option for successful detection. Comparison between different dyes is stated in Table 1 according to the SGO consensus27.

In addition to tracker dyes, injection positions also affect detection rates of SLN mapping. Dye injection in the cervix cannot wholly reflect the lymphatic drainage, though the procedure is relatively simple and popular in clinical trials28,29. A hysteroscopic injection requires more skill and is located near the tumor lesion. The myometrial site is challenging to access intraoperatively, resulting in a low negative predictive rate of 87.50% and a false-negative rate of 33.30%30. In studies using cervical injection, the sensitivity range was 62.5%-97.5%, while myometrium injection was 66.70%-94.10%31. A systematic review including 55 eligible studies revealed an overall detection rate of 81% (95% confidence interval is from 77 to 84)32. Double detection works better than single detection, regardless of the injection location33. In the ongoing clinical study (NCT04276532), where 92 EC patients were enrolled, the SLN mapping detection rate was as high as 91.3%, with a total sensitivity of 73.3%. Combining cervical and fundus injections reached a higher para-aortic detection rate (40.4%) than cervical injections alone (4.4%), indicating that the combined injection is more efficient.

There are many possible reasons for insufficient SLN detection. Anatomically, the Naboth cyst and postsurgical abnormal pelvis affect mapping accuracy. Excessive adipose tissue near the cervix and cervical stenosis due to aging also lead to failed mapping. Factors such as body mass index (BMI), ISB dye use, and enlarged nodes are associated with SLN mapping failure34. Controversially, one prospective study including 110 EC patients reported that obesity and the presence of lymph node metastases were not associated with detection failure35. Lymphovascular space invasion might lead to failure of SLN mapping as well.

International guidelines consider SLN mapping and biopsy as necessary procedures10,18. However, there are debates about whether to conduct SLN mapping in intermediate-high risk EC patients. Patients with severe carcinoma, clear cell carcinoma, and carcinosarcoma have a higher risk of node metastasis36. On the contrary, some trials have determined that SLN mapping is a safe alternative to systematic lymphadenectomy because of lower complication occurrence37,38 and equivalent overall survival37. More high-quality clinical trials are required to determine the optimal inclusion standards.

In conclusion, SLN mapping and biopsy are better options than systematic lymphadenectomy to make the operation as simple and minimally invasive as possible. It can even improve the pathological stage of the disease by using a pathological ultrastaging method to guide the postoperative adjuvant therapy more accurately. For maximizing the specificity and sensitivity of SLN detection, this protocol provides tips for SLN mapping and biopsy to ensure a better outcome of the surgery.

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Disclosures

The authors have nothing to disclose.

Acknowledgments

This work was supported in part by grants from the National Natural Science Foundation of China (81772777), Shanghai Science and Technology Commission Medical Guidance Project (18411963700), Clinical Research Plan of SHDC (No. SHDC2020CR4079); Shanghai Pujiang Talents Project (17PJ1401400). We thank the timely help given by Fenghua Ma from radiology department for MR images and Chao Wang from pathology department for pathologic images from Obstetrics and Gynecology Hospital of Fudan University.

Materials

Name Company Catalog Number Comments
2-mL syringe Becton, Dickinson and Company, USA 301940
Coagulation forceps Shanghai Medical Instrument (Group) Co., Ltd. Surgical Instrument Factory D0A010
Fluorescence microscope Olympus IX73
Harmonic scalpel Soering GmbH SONOCA190
Hematoxylin-eosin staining Beyotime Biotechnologies Corporation,CN C0107
Immunohistochemical cytokeratin staining MXB Biotechnologies Corporation, CN Kit-0020
Indocyanine green (ICG) Dandong Medical Innovation Pharmaceutical Corporation. 3599-32-4
Pararaffin Sangon biotech Co., Ltd. A601889
Pinpoint Endoscopic Fluorescence Imaging system Novadaq Technoloies Bonita, Springs, FL NA
Propofol Injection Fresenius Kabi Deutschland GmbH D-61346 Bad Homburg v.d.H., Germany H20030124
Silk Braided non-absorbable suture Shanghai Ethicon SA854G
Silk thread Beijing AKIN AIEN International Medical Technology Co.,Ltd. VCPP71D
Suction-Irrigation Tube Shanghai SMAF YX980D
Toothless forceps Shanghai Medical Instrument (Group) Co., Ltd. Surgical Instrument Factory J41010
Trocar ETHICON Co,. Ltd, USA B10LT, B5LT

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Tags

Sentinel Lymph Node Mapping Biopsy Endometrial Cancer Early Stage Laparoscopy Minimally Invasive Complications Medical Costs Detection Rate Lymph Node Metastases Pathological Ultrastaging SLN Mapping Learning Curve Injection Cervix First Mapped Lymph Node Case Anesthetizing Umbilicus Abdominal Wall Incision Fascia Peritoneum Trocar Pneumoperitoneum Laparoscope Small Incisions Lower Abdomen Instruments For Manipulation Fallopian Tubes
Sentinel Lymph Node Mapping and Biopsy for Endometrial Cancer at Early Stage with Laparoscopy
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Cite this Article

Wang, B., Xue, Y., Wang, Q., Xu, Y., … More

Wang, B., Xue, Y., Wang, Q., Xu, Y., Chen, X., Wang, C. Sentinel Lymph Node Mapping and Biopsy for Endometrial Cancer at Early Stage with Laparoscopy. J. Vis. Exp. (174), e63044, doi:10.3791/63044 (2021).

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