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Annals of Surgical Oncology 9:550-554 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Validation of Sentinel Node Mapping in Patients With Colon Cancer

Juan C. Paramo, MD, Janna Summerall, MD, Robert Poppiti, MD and Thomas W. Mesko, MD, FACS

From the Departments of Surgery (JCP, TWM) and Pathology (JS, RP), Mount Sinai Medical Center, Miami Beach, Florida.

Correspondence: Address correspondence and reprint requests to: Juan C. Paramo, MD, Department of Surgery/Section of Surgical Oncology, Mount Sinai Medical Center, 4300 Alton Road, Miami Beach, FL 33140; Fax: 305-674-2863; E-mail: jcparamo{at}med411.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Sentinel lymph node (SLN) mapping techniques have been validated in breast cancer and melanoma. This study summarizes our experience with SLN mapping for colon cancer.

Methods: Fifty-five patients with colon cancer underwent intraoperative SLN mapping. One mL of 1% isosulfan blue was injected subserosally around the tumor. The first nodes highlighted with blue were identified as the SLNs. SLNs underwent multiple sectioning and immunohistochemical staining for cytokeratin. The overall learning curve was calculated.

Results: Lymphatic mapping adequately identified at least 1 SLN in 45 patients (82%). SLNs adequately predicted regional status in 44 of 45 (98%) cases. In 9 of 45 cases (20%), the SLNs were the only sites of metastases. Among the 14 cases that were SLN positive, 6 of 55 patients (11%) were positive only by immunohistochemistry. Of the 31 cases with negative SLNs, 1 case had a 3.5-mm pericolonic tumor-replaced non-SLN (3% false-negative rate). The overall learning curve stabilized after five cases.

Conclusions: Intraoperative SLN mapping is a feasible technique, with a quick learning curve, and had a reasonable SLN identification rate. Negative SLNs accurately predict the status of non-SLNs 97% of the time. Eleven percent of patients were upstaged by demonstration of micrometastases and may benefit from adjuvant chemotherapy.

Key Words: Sentinel lymph node mapping • Colon cancer • Staging • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Colorectal cancer is the third most common cause of cancer-related mortality in the United States.1 The development of locoregional recurrences and distant metastases accounts for most of these deaths. Adequate tumor staging, including evaluation of the presence of regional lymph node metastases at the time of diagnosis, is essential, because it constitutes the most important prognostic factor.2

In an attempt to improve the accuracy of the staging of the regional nodes, the sentinel lymph node (SLN) mapping technique was developed. According to the SLN concept, metastatic tumor cells will progress from the primary tumor in an orderly and sequential fashion, following the lymphatic channels into the most direct site of drainage, known as the SLN.3–5 Once the SLN is identified, it can undergo a detailed pathologic examination to identify metastatic disease.6–8 Because the SLN is the first site of lymphatic drainage, it is at greatest risk for harboring metastases and should accurately predict the status of the regional lymph nodes.9,10

Intraoperative SLN mapping has been used in patients with primary melanoma and breast cancer and was found to be a very accurate staging procedure.11–16 The SLN concept was subsequently found to be applicable for solid neoplasms, including colorectal cancer.3,9,17,18

This study represents a continuation of our initial pilot study.18 The purpose was to validate the technique of SLN mapping in patients with colon cancer. The diagnosis of nodal metastases would upstage a group of these patients, who may benefit from adjuvant chemotherapy.3,10


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Between June 1999 and August 2001, 55 patients with endoscopic biopsy-proven colon adenocarcinoma were included in a prospective fashion. Seven attending surgeons were selected to participate in the study. The study was conducted with an institutional review board–approved protocol.

Patient characteristics, including age, sex, and tumor location, were documented. Preoperative staging evaluation included physical examination, liver function tests, chest x-ray, computed tomography of the abdomen and pelvis, and colonoscopy in all patients. Patients with preoperative or intraoperative evidence of distant metastatic disease outside of the colonic regional lymph nodes were excluded from the study. Likewise, patients with rectal carcinoma were excluded.

Patients were brought to the operating room, where an exploratory laparotomy was performed and the location of the carcinoma was identified. The colon adjacent to the tumor was then mobilized carefully; we tried to minimize dissection or manipulation of the mesentery. Once the primary lesion was isolated, 1 mL of 1% isosulfan blue (LymphazurinTM; BenVenue Laboratories Inc., Bedford, OH) was injected subserosally circumferentially around the tumor by using a tuberculin syringe.3,10

Within the first 5 minutes after injection, the first to fourth nodes that were highlighted with blue were identified as the SLNs and were marked with a stitch. Standard oncological en-block resection was then performed.

The surgical specimen was sent fresh to the pathology department, where the SLNs were again identified. The SLNs were submitted in their entirety for microscopic examination and, depending on their size, were bisected or sectioned at 2- to 3-mm intervals. Paraffin-embedded, formalin-fixed tissue blocks were cut at a thickness of 4 µm and stained with hematoxylin and eosin (H&E). If these were found to be negative on initial H&E evaluation, five additional deeper sections were obtained from the SLNs at 20-µm intervals and stained with low-molecular-weight cytokeratin (Cam 5.2TM, 1:2; Becton Dickinson, San Jose, CA). The remainder of the surgical specimen was then dissected to identify other lymph nodes contained in the mesentery. These nodes underwent routine histological evaluation with H&E. The T stage per the American Joint Committee on Cancer (AJCC),19 the number of nodes, and the number of positive nodes were recorded.

The learning curve for each individual surgeon was calculated according to the SLN detection rate for each sequential case performed. An average curve rate was then created to reflect the percentage of SLN detection for each consecutive case.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Twenty-eight men and 27 women were studied. The average age was 70 years (range, 27 to 98 years). The primary tumor was located in the right colon in 34 cases, splenic flexure in 2, left colon in 9, and sigmoid colon in 10. Eight tumors were T1, 6 were T2, and 41 were T3. No patient had previous colon surgery.

A total of 664 nodes were evaluated, with an average of 12 per patient. Lymphatic mapping adequately identified at least 1 SLN in 45 of 55 patients (82%). A total of 87 SLNs were studied. SLNs adequately predicted the status of regional nodes in 44 of 45 (98%) cases. One SLN was found in 20 patients, 2 SLNs in 14 patients, 3 SLNs in 5 patients, and 4 SLNs in 6 patients.

No metastases were found in the SLNs of 31 patients. Of these 31 cases, all other non-SLNs were also negative for metastatic involvement in 30 patients. The one other patient had a microscopic 3.5-mm pericolonic nodule interpreted as a tumor-replaced non-SLN (3% false-negative rate).

The SLNs were positive for metastases in 14 patients. Among these cases, the SLNs were the only site of metastasis in 9 patients (16% of the total of 55 patients); in these 9 patients, the size of the SLNs ranged from 0.5 to 1.2 cm. Thirty-six percent of patients with positive SLNs also had other positive regional lymph nodes. Of the 14 patients with positive SLNs, additional sectioning and staining with CAM 5.2 provided the only positive evidence of metastasis in 6 cases (11% of the total of 55 patients; Fig. 1). Patterns and distribution of metastases are listed in Table 1.



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  		FIG. 1. Photomicrograph of a lymph node initially negative by hematoxylin and eosin but found to harbor micrometastases by immunohistochemistry.

 

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  		TABLE 1. TABLE 1. Patterns and distribution of metastases
 
In one patient, aberrant lymphatic drainage (ALD) was identified. The primary tumor was located in the ascending colon, and the SLN was found just distal to the origin of the middle colic vessels. An extended right colectomy was performed without complications. The SLN was the only positive node by H&E examination.

There were no complications specifically related to the SLN technique in any of the 55 cases. The average learning curve stabilized after five cases, when an almost 100% SLN detection rate was achieved (Fig. 2).



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  		FIG. 2. Average learning curve for sentinel lymph node (SLN) detection according to the sequential number of cases performed.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Approximately 55% of patients with colorectal cancers present initially with disease confined to the wall of the bowel and no evidence of nodal metastases (stage I or II per the AJCC).10,19 Unfortunately, 20% to 30% of these patients will experience recurrence of their disease and die of metastatic disease within 5 years of diagnosis, despite undergoing curative surgery.20 A possible explanation of this high mortality rate is that conventional methods underestimate micrometastatic nodal involvement. Foci of micrometastases are often located in the subcapsular sinus of a lymph node and can be missed by the conventional pathologic examination, which is limited to one or two sections.10 Alternative diagnostic techniques need to be developed to better stage patients with colorectal cancer at the time of initial diagnosis, because adequate staging is the most important prognostic factor, and the presence of lymph node metastases decreases the 5-year survival by approximately 20% to 30%.2,3

Several methods described below have been studied in an attempt to increase the yield of diagnosis of micrometastases. However, serial sectioning of all lymph nodes found in the surgical specimen is time consuming and tedious21 and, if combined with immunohistochemical (IH) staining6,22,23 or reverse transcriptase-polymerase chain reaction,24 becomes very expensive. Because up to 69% of metastatic nodes are <5 mm in size, unless meticulous fat-clearing techniques are used, metastatic disease can be easily missed.25,26 The SLN mapping technique attempts to address all these problems and limitations.

The SLN concept is based on an organized progression of tumor cells from the primary tumor site into the regional lymph nodes. This process has been validated in melanoma and documented in patients with breast cancer.4,14–16,25 Once the SLN has been identified, a dedicated cost-effective evaluation of the SLN can be performed. If the SLN concept is true, the status of the SLN should accurately predict the metastatic involvement of the regional nodal basin.

Typically, patients with stage I or II colon cancer would not be treated with chemotherapy outside of a protocol. It has been postulated, and we concur, that patients with micrometastases should be upstaged from AJCC stage I or II to stage III. Previous studies using the SLN mapping technique have upstaged 11% to 20% of patients with colorectal cancer from stages I and II to stage III disease.3,9,10,18 Nodal micrometastases were identified in 8% to 18% of patients when multisectioning and IH evaluation of the SLNs were performed.3,9,10 These results were corroborated in our study, in which the SLN was the only node containing metastatic disease in 16% of patients and IH stains upstaged 11% of all patients by demonstrating micrometastatic involvement. It is reasonable to believe that this subset of patients that can be identified with the SLN technique may benefit from adjuvant systemic therapy.10 Whether such therapy prolongs the survival of these patients with micrometastases remains to be seen.

In colon cancer, en-block resection and formal lymphadenectomy is still the standard of care. Contrary to in melanoma and breast cancer, the SLN technique in colon cancer is not intended to minimize the need for therapeutic lymphadenectomy. In our study, 36% of patients with positive SLNs also had other positive regional lymph nodes. Therefore, the main role of the SLN technique for colon cancer is not to decrease the amount of mesenteric dissection, but to improve the accuracy of nodal staging. This is corroborated by the fact that the SLN adequately predicted the regional status in 98% of our cases. In addition, among the nine (16%) patients who were only SLN positive, routine pathologic sampling may have missed four metastatic nodes because they were only 0.5 cm in size. The 3% false-negative rate in our study also compares favorably with that in other studies that document a 0.6% to 10% rate.3,9,27,28

In our study, one patient was found to have ALD. The SLN was also the only positive metastatic node in this patient. Other studies have reported ALD in 2% to 14% of cases of colorectal cancer.3,9,10,29 We believe that if ALD is identified, a more radical surgical resection should be performed, to include a complete lymphadenectomy of the SLN-bearing nodal basin. Whether ALD is a significant source of inadequate staging, higher recurrence rates, and decreased overall survival needs to be determined in future studies.

The calculated overall learning curve shows that an almost 100% SLN detection rate can be achieved after five cases (Fig. 2). Because this was a multisurgeon study, the 82% total SLN identification rate is a reflection of the initial learning curve experience. Other authors have reported SLN detection rates of 70% to 98%.3,9,10,30 Some of the pitfalls that may account for an inadequate SLN identification rate include incomplete circumferential injection of the dye around the tumor, intraluminal rather than subserosal injections, large tumors that may require larger amounts of dye to achieve complete peritumoral injection, obstruction of the lymphatic channels in nodes that are completely replaced by tumor and therefore prevent adequate flow of the dye, and patients with previous colon surgery that may alter the lymphatic flow patterns.10

In this study, we used isosulfan blue exclusively as the staining dye. Isosulfan blue is inexpensive, is easy to use, and is readily seen as it travels through the mesenteric lymphatics. The use of radioactive colloid in colon cancer, injected either before or during surgery, we believe to be cumbersome and impractical. The colloid additionally has radiation-related risks and is more expensive than isosulfan blue.

We excluded patients with rectal tumors because we believe that application of the SLN technique in the rectum is limited. The mesorectum needs to be dissected from the pelvic cavity before the tumor can be mobilized adequately to allow peritumoral injection. This potentially alters the lymphatic drainage pattern. Other reported series have shown a lower SLN identification rate in rectal cancer.9


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Intraoperative SLN mapping is feasible and safe and has a quick learning curve. SLN examination is highly accurate, because it adequately predicts the regional status in 98% of cases. The absence of metastases in the SLN accurately predicts the status of the non-SLNs 97% of the time. The SLN technique improves the staging of patients with colon cancer by upstaging 11% of patients, who may benefit from further adjuvant chemotherapy. Implications for long-term survival and prognosis need to be further evaluated in additional studies.

Received for publication December 19, 2001. Accepted for publication March 29, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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