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10.1245/s10434-006-9038-4
Annals of Surgical Oncology 13:1168-1174 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Sentinel Node Biopsy Using Dye and Isotope Double Tracers in Early Gastric Cancer

Jun Ho Lee, MD, Keun Won Ryu, MD, Chan Gyoo Kim, MD, Seok-Ki Kim, MD, Jong-Seok Lee, MD, Myeong-Cherl Kook, MD, Il Ju Choi, MD, Young Woo Kim, MD, Hee Jin Chang, MD and Jae-Moon Bae, MD

Research Institute and Hospital, National Cancer Center, 809 Madu1-dong, Ilsandong-gu, Goyang-si, Gyeonggi-do410-769, South Korea

Correspondence: Address correspondence and reprint requests to: Keun Won Ryu, MD; E-mail: docryu{at}korea.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The results of sentinel node (SN) biopsy have been improved by the use of dye and isotope double tracers in melanoma and breast cancer. However, the usefulness of this double tracer technique has not been determined in gastric cancer. The aim of this study was to investigate the possibility of improving SN biopsy results by using double tracers in gastric cancer.

Methods: Sixty-four gastric adenocarcinoma patients preoperatively diagnosed as cT1N0, were enrolled in the study. 99mTc tin colloid was injected by preoperative endoscopy, and lymphoscintigraphy was performed prior to operation. After laparotomy, isosulfan blue was intraoperatively injected using an endoscope. Blue-stained or radioactive nodes were identified and defined as SNs. Gastrectomy with D2 lymphadenectomy was performed in all patients. All dissected lymph nodes were evaluated for metastasis by hematoxylin and eosin staining and immunohistochemistry.

Results: SN detection rates using dye, isotope, or both tracers were 95.3%, 84.4%, and 96.9%, respectively, and their corresponding sensitivities were 52.9%, 52.9%, and 70.6%. In the pT1 subset, the sensitivity of the double tracer was 87.5%; and in a subset of tumors with diameter <4.5 cm, this was also 87.5%.

Conclusions: These findings confirm that SN biopsy results are improved by using double tracers in gastric cancer and suggest that SN biopsy is suitable in cases of small-sized early gastric cancer.

Key Words: Sentinel node • Gastric cancer • Dye • Isotope


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Gastrectomy with D2 lymphadenectomy is the standard surgical procedure in gastric cancer because lymph node metastasis, along with the depth of primary tumor invasion, is an important prognostic factor.1 The incidence of lymph node metastasis is low in early gastric cancer (EGC) patients, who have a 5-year survival rate of >90%.2 Recently, various minimally invasive procedures like endoscopic mucosal resection and laparoscopic wedge resection without lymph node dissection have been performed in selected EGC patients to improve the quality of life of long-term survivors.3,4 For such procedures, the accurate prediction of lymph node metastasis is crucial to determining the extent of lymph node dissection. However, current diagnostic imaging techniques are unsatisfactory for accurately predicting lymph node metastasis.

The sentinel nodes (SNs) are the first possible site of metastasis via lymphatic drainage from a primary tumor; this was initially proposed for malignant parotid tumors by Gould et al.5 Moreover, the absence of metastasis in SNs is believed to be correlated with the absence of metastasis in downstream lymph nodes. This concept has been evaluated in various tumors, and the prediction of node status in melanoma and breast cancer by SN biopsy has produced promising results.6,7 However, SN biopsy in gastric cancer is practiced more cautiously because lymphatic drainage from the stomach is much more complicated and because skip metastasis seems more common in gastric cancer.8,9 Although recent studies have shown the feasibility of SN biopsy in gastric cancer, results have been unsatisfactory for clinical applications in terms of sensitivity.10,11

Dye and isotope are commonly used SN biopsy tracers. They have several advantages and disadvantages with respect to each other in terms of their kinetics in the lymphatic system, convenience, cost, and associated side effects.11 In melanoma and breast cancer, SN biopsy using combined dye and isotope produced improved results, and it has been suggested that these tracers are complementary.12,13 However, few studies on the use of dye plus isotope as double tracers for SN biopsy have been performed in gastric cancer. Therefore, this study was conducted to verify that the use of dye and isotope tracers in gastric cancer improves the results of SN biopsy.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients and Eligibility
From July 2003 to December 2004, 64 gastric adenocarcinoma patients diagnosed as cT1N0 with tumor <5 cm in diameter, based on preoperative evaluation, were prospectively enrolled in this study. Preoperative evaluation included esophagogastroduodenoscopy, abdominal computed tomography, a chest X-ray, and a basic blood test. Endoscopic ultrasound was not used because its accuracy for tumor staging in routine clinical use has been reported to be low.14 Well-differentiated mucosal tumors <2 cm without an ulcer were excluded for endoscopic mucosal resection, in accord with the treatment guidelines of our institution and Japanese guidelines.15 In addition, patients with a history of an allergic reaction to medications, abdominal surgery, or radiation were excluded. Patient recruitment and sample collections were performed according to the protocol guidelines approved by our institutional review board, and informed consent was obtained from all patients.

Procedures
99mTc tin colloid was reconstituted by adding 2 mL of sterile sodium pertechnetate [99mTc] at a radioactive concentration of 10 mCi/mL into tin (II) chloride solution (Korea Atomic Energy Research Institute, Daejeon, South Korea). The tin colloid solution was filtered through a 0.45 µm syringe filter (Millipore, Bedford MA) and the radioactivity was adjusted to 1 mCi/mL by adding normal saline. Four to 16 hours before operation, 99mTc tin colloid (2 mL, 2 mCi) was endoscopically injected into four sites of the gastric submucosa around the tumor, as Kitagawa et al.16 Lymphoscintigraphy was performed before operation to confirm adequate injection of isotope and to identify SNs. After completing laparotomy and whole-abdomen exploration, the proximal jejunum was occluded with an intestinal clamp to prevent overflow of inflated gastric air during intraoperative endoscopy. One milliliter of 1% isosulfan blue was injected into four sites around the tumor submucosally using an intraoperative endoscope. After completing the endoscopic injection, the intestinal clamp was declamped and removed. No form of massage was performed on the stomach during the procedures. Five minutes after dye injection, the omental bursa was opened near the transverse colon and blue-stained lymph nodes were identified and defined as blue SNs, as decribed in our previous study.17 Blue SNs were marked with a suture to facilitate identification after resection. Radioactivity was monitored using the hand-held gamma probe (Navigator®, Gamma Guidance Systems, USSC, RMD Waterton, MA, USA) in all abdominal cavities, including the perigastric, celiac, perisplenic, and hepatoduodenal areas. Gamma probe was placed perpendicular to the suspected hot SNs at as short a distance as possible. Also, it was directed opposite from the primary tumor as possible, to avoid the radiation from the primary tumor. A thick lead plate was applied at the primary tumor to shield radiation from the primary tumor (Fig. 1Go). Lymph nodes with radioactivity levels 10 times that of the background were defined as hot SNs and marked with a suture distinguishable from those used for blue SNs. Gastrectomy with D2 lymphadenectomy was performed according to the Japanese gastric carcinoma classification.18 Hot SNs not identified before resection were identified on a back table after resection.


Figure 1
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  		FIG. 1. Intraoperative detection of hot SNs.

 
Pathologic Evaluation
All dissected lymph nodes were sliced at 2 mm intervals and stained with hematoxylineosin (H-E) and prepared for immunohistochemistry (IHC) using pan-cytokeratin antibody (1:50, cytokeratin, mouse anti-human cytokeratin, monoclonal, clone AE1/AE3, IgG1-kappa, M3515; Dako Cytomation, Carpinteria, CA). Metastatic findings of H-E staining and IHC were interpreted by different pathologists (M. C. K. and H. J. C.). Cancer staging was performed according to the American Joint Committee on Cancer guidelines.19

Statistical Analysis
The results of SN biopsies were quantified in terms of detection rate, sensitivity, specificity, positive predictive value, negative predictive value, and accuracy.20 These were compared for dye, isotope, and double tracers using the Mann-Whitney U-test for continuous variables and Fisher’s exact test for categorical variables. P values were two-sided, and values <0.05 were considered statistically significant. All data were analyzed using SPSS version 9.0 (SPSS Inc., Chicago, IL). A biostatistician approved all statistical procedures.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Clinicopathologic Characteristics of the Enrolled Patients
Details of the 64 study subjects are listed in Table 1Go. The majority of patients were male (81.3%), and the average age was 60.0 years. Average tumor size (± standard deviation [SD]), based on longest diameter, was 3.5 ± 2.1 cm. The number of patients with pT1 was 53 (82.8%) and that with pT2 was 10 (15.6%). One case (1.6%) with tumor cells invading the serosa microscopically was diagnosed as pT3. The average number of dissected lymph nodes was 28.5 ± 9.1, and lymph node metastasis was observed in 17 patients (26.6%). In the pT1 subset (n = 53), lymph node metastasis was observed in eight patients (15.1%); and in the pT2 subset (n = 10), it was observed in eight patients (80.0%).


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  		TABLE 1. Clinicopathologic characteristics of enrolled patients (n = 64)
 
SN Biopsy Algorithm
SNs were identified in 62 of the 64 subjects (96.9%) using double tracers (Fig. 2Go), and the average number of SNs was 4.1 ± 2.0. In the two failed cases, blue-stained SNs were not identified due to faulty dye injection into the interstitial space and consequent staining of all perigastric tissues. Hot SNs were not identified even though radioactivity was high in the primary tumor. Of the patients identified as having SNs, metastatic SNs were found in 12 of the 62 using double tracers. Metastasis in non-SNs was also found in 5 of these 12 patients (41.7%). No metastasis was found in non-SNs in 45 of 50 patients (90.0%) with nonmetastatic SNs identified by double tracers. Double tracer SN biopsy precisely diagnosed lymph node metastasis in 12 of 17 patients (70.6%).


Figure 2
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  		FIG. 2. Algorithm of SN biopsy.

 
Hot SNs were not detected by preoperative lymphoscintigraphy. In most cases, it was found that radioactivity from hot SNs was masked by strong radioactivity from the primary tumor (Fig. 3AGo). In one patient, isotope collected in the gallbladder and in the primary tumor (Fig. 3BGo). Isotope spillage was also well visualized along the gastrointestinal tract in one patient (Fig. 3CGo). Before specimen resection in all cases, no hot SN was identified with a hand-held gamma probe due to strong background radiation from the primary tumor, even though a thick lead plate was used. Therefore, hot SNs were harvested at the back table just after resection in all patients.


Figure 3
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  		FIG. 3. Lymphoscintigraphy before operation. (A) Usual patterns. (B) Isotope uptake in gallbladder. (C) Isotope spillage in gastrointestinal tract.

 
Comparisons of SN Biopsy Results
SN detection rate was significantly improved by double tracers vs. isotopes alone (96.9% vs. 84.4%, P = 0.030) (Table 2Go). Mean SN numbers using both tracers were significantly greater than for dye (2.2 ± 1.2 vs. 4.1 ± 2.0, P < 0.001) or isotope (3.0 ± 1.6 vs. 4.1 ± 2.0, P = 0.002). SN biopsy sensitivity was also greater for double tracers than for dye (70.6% vs. 52.9%) or isotope (70.6% vs. 52.9%).


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  		TABLE 2. Comparison of SN biopsy results with dye and isotope
 
Analysis of False-Negative Cases
False-negative SN biopsies occurred in five cases using double tracers (Table 3Go). Two cases occurred in the early half of the study and three cases in the later half. In four cases, metastatic lymph nodes were located at the same station as the SNs according to the Japanese Gastric Cancer Classification.18 Metastatic non-SNs of case 4 were located at different station from SNs (Fig. 4Go). One patient had a primary pT1 tumor and the others had a pT2 tumor. With the exception of one case, four false-negative cases had a tumor size >4.5 cm. In those with a pT1 tumor, seven of eight patients with metastasis were diagnosed by double tracer SN biopsy (sensitivity 87.5%). However, in pT2 cases, only four of eight patients with metastasis were diagnosed (sensitivity 50%). Also, in those with a tumor <4.5 cm, seven of the eight patients with metastasis were diagnosed by double tracer SN biopsy (sensitivity 87.5%). However, in those with tumors ≥4.5 cm, only five of the nine patients with metastasis were diagnosed (sensitivity 55.6%).


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  		TABLE 3. Details of five false-negative cases of SN biopsy with double tracers of dye and isotope
 

Figure 4
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  		FIG. 4. Profile of case 4, false-negatives.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The clinical application of SN biopsy in gastric cancer requires that its detection rate and sensitivity should be sufficiently high to minimize false-negative cases. However, available data on SN biopsies show higher levels of false-negatives in gastric cancer than melanoma or breast cancer.10,11 Combinations of dye and isotope have been used to improve SN biopsy results in melanoma, breast, and colorectal cancers.12,13,21 The present study indicates that the double tracer SN biopsy technique also improves results in gastric cancer. With regard to detection rates, this technique offered a significant improvement over the use of isotope alone. Sensitivity was also improved using double tracers, but this finding was not statistically significant due to the small number of lymph node-positive patients. We are confident that had more patients with lymph node metastasis been enrolled it would have been statistically significant.

Even though sensitivity was improved by the use of double tracers, it was still insufficient for clinical application. The lower sensitivity in this series compared to other reports might be attributed to several factors. First of all, it might be a technical issue. Even though this study was a single-center trial under strict protocol, four surgeons and three endoscopists were involved. Personal technical differences might have affected the results. A second point is the pick-up SN biopsy rather than basin dissection. We chose the pick-up biopsy technique for practical reasons because basin dissection might result in many SNs and it takes a long time for intraoperative pathologic confirmation. Most studies on SN biopsy in gastric cancer have used the basin dissection technique and reported sensitivity of around 90%.22

When we analyzed the five false-negative cases, they had either deeper tumor infiltration or a large tumor size. Double tracer sensitivity was 87.5% for pT1 lesions but only 50.0% for pT2. We are uncertain why advanced tumors showed such low sensitivity. Some investigators have suggested that such false-negatives are due to lymphatic vessel obstruction by the tumor; however, others have claimed no relationship with tumor burden.23,24 With regard to tumor diameter, double tracer sensitivity was 87.5% for tumors with a diameter <4.5 cm but 55.6% for tumors with a diameter ≥4.5 cm. We presume that deeper and larger tumors have more diverse directions of lymphatic metastasis and that this resulted in false-negative cases by SN biopsy. These findings suggest that small EGCs are suitable for SN biopsy.

In case 4, metastatic non-SNs were located at a different lymphatic basin from SNs and it was supposed that isotope and dye were injected inadequately. Other than this case, metastatic nodes were located at the same station as SNs in other false-negative cases. Therefore, lymphatic basin dissection rather than pick-up SN biopsy may improve sensitivity in gastric cancer.22 The usefulness of preoperative lymphoscintigraphy has been well studied in melanoma and breast cancer.25,26 However, in the present study, hot SNs were not identified by lymphoscintigraphy. Usually, SNs in gastric cancer are located close to the primary tumor, and the strong radioactivity emitted by the primary tumor interferes with the visualization of radioactivity emitted by hot SNs. Seventeen hours postinjection, 83% of the original activity remained at the injection site and radioactivity accumulating at single lymph node ranged 0.01–1%.27 Nevertheless, despite these shortcomings, lymphoscintigraphy usefully identified abnormal site uptake and gastrointestinal spillage. Hot SN detection using a hand-held gamma probe before resection was not possible for the above-mentioned reasons, even with the use of a lead plate shield on the primary tumor. The so-called shine-through phenomenon is regarded as a major obstacle in SN biopies using isotopes.21,28

In the present study, the detection rate obtained using isotope alone was lower than that reported by other studies.16,29 Concerning the isotope preparation and injection method, we referenced previously published work. Kitagawa et al.16 reported that injected 99mTc tin colloid with a relatively large particle size stayed in SN steadily from 2 to 16 hours and that there was no relationship between the interval of injection of radiocolloid to the SN harvest and the number of identified SNs. We used 99mTc tin colloid, which has a relatively large particle size with a mean diameter of around 500 nm. Some authors have reported good results for this same isotope, while others have recommended the use of radiocolloids with a particle size of 100 nm to increase uptake in gastric cancer, which may explain the low detection rate observed in the present study.30

We conclude that SN biopsy detection rates and sensitivities can be improved by using the dye and isotope double tracer technique. In addition, our findings suggest that SN biopsy is a suitable modality in small EGCs.


   ACKNOWLEDGMENTS
 
This work was supported by grant 0310020 from the National Cancer Center, South Korea. The authors thank Dr. Byung-Ho Nam (Cancer Biostatistics Branch, National Cancer Center, South Korea) for statistical revision of the manuscript.

Received for publication October 28, 2005. Accepted for publication March 18, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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