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Annals of Surgical Oncology 8:821-827 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Utility of Breast Sentinel Lymph Node Biopsy Using Day-Before-Surgery Injection of High-Dose 99mTc-Labeled Sulfur Colloid

Carmen C. Solorzano, MD, Merrick I. Ross, MD, Ebrahim Delpassand, MD, Nadeem Mirza, MD, Jeri S. Akins, MPAS, PAC, Henry M. Kuerer, MD, PhD, Funda Meric, MD, Frederick C. Ames, MD, Lisa Newman, MD, Barry Feig, MD, S. Eva Singletary, MD and Kelly K. Hunt, MD

From the Departments of Surgical Oncology (CCS, MIR, NM, JA, HMK, FM, FCA, LN, BF, SES, KKH) and Diagnostic Radiology (ED), The University of Texas M. D. Anderson Cancer Center, Houston, Texas.

Correspondence: Address correspondence and reprint requests to: Kelly K. Hunt, MD, M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Box 444, Houston, TX 77030; Fax: 713-792-4689; E-mail: khunt{at}mail.mdanderson.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: In sentinel lymph node (SLN) biopsy for breast cancer, many centers use same-day preoperative injection of technetium 99mTc-labeled sulfur colloid and intraoperative injection of blue dye for localization of SLNs. Same-day sulfur colloid injections can be problematic because of the variability in sulfur colloid migration times, which can lead to ineffective use of operating room time, and low SLN-to-background radioactivity ratios. We examined the utility of day-before-surgery injections of high dose 99mTc-labeled sulfur colloid injections.

Methods: The day before surgery, high-dose 99mTc-labeled sulfur colloid was injected peritumorally, and a lymphoscintigram was obtained. Intraoperatively, after injection of blue dye, a gamma probe was used to localize SLNs. Nodes that were stained blue or were highly radioactive were considered SLNs and were removed.

Results: Lymphoscintigraphy demonstrated drainage in 107 patients (91%). Transcutaneous localization of the SLN was possible in 104 patients (89%). In three patients, all of whom had no drainage demonstrated on lymphoscintigraphy, no SLN was identified at surgery (97.5% success rate for SLN identification). A mean of 2.3 SLNs per patient were identified. Twenty-five patients (21%) had at least one histologically positive SLN. In 23 of these patients, the positive SLN was the SLN with the most radioactivity, and in the remaining two patients, the positive SLN was both blue-stained and hot.

Conclusion: Day-before-surgery injection of high-dose 99mTc-labeled sulfur colloid results in high rates of transcutaneous and intraoperative identification of SLNs. The delay between injection and surgery did not appear to promote significant passage of sulfur colloid to second-echelon nodes.

Key Words: Technetium 99m • Sulfur colloid • Biopsy • Sentinel lymph node • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Axillary lymph node dissection has been used routinely for the staging and locoregional treatment of breast cancer patients. In 1991, a National Institutes of Health consensus development conference recommended the routine use of level I and II axillary lymphadenectomy, largely on the basis of studies from the 1980s.1 Recently, this standard of care has been called into question. Increased awareness of disease and screening for breast cancer have led to a rise in the proportion of patients presenting with early-stage disease, the same patients in whom axillary dissection usually fails to yield positive lymph nodes.2–4 In addition, the morbidity of an axillary dissection can be substantial.5 The desire to achieve a balance between the benefits and the morbidity of axillary dissection provided the impetus for attempts to develop new and less invasive techniques for evaluating the axillary nodes.

In the 1970s, Cabanas introduced the concept of the "sentinel lymph node" (SLN) while working on penile cancer.6 Subsequently, Morton and colleagues validated the SLN concept using skin injections of vital blue dye in patients with melanoma and named this procedure lymphatic mapping.7 To help guide surgeons to SLNs in patients with breast cancer, Krag and colleagues advocated the use of radioactive colloid injections; they described a technique in which the surgeon uses a handheld gamma probe to find areas of high radioactivity ("hot spots"), which correspond to lymph nodes. Surgeons are then guided toward the radioactive node by following the "line of sight."8,9 Giuliano and colleagues adapted the concept of mapping with blue dye that had been introduced by Morton and colleagues for melanoma for use in patients with breast cancer.10,11 When radioactive colloid is used, a preoperative lymphoscintigram often is obtained to ease SLN identification further. Numerous studies using injection of radioactive colloid (with or without a lymphoscintigram), blue dye, or both have demonstrated that these techniques permit successful identification of SLNs and accurate staging of early-stage operable breast cancer.10,12–21 Although these techniques have been successful, they are still evolving, and SLN biopsy is not yet considered the standard of care in breast cancer.20,22,23

In many centers, patients scheduled to undergo SLN biopsy for breast cancer routinely undergo same-day preoperative injection of 99mTc-labeled sulfur colloid and intraoperative injection of blue dye. Same-day injections of 99mTc-labeled sulfur colloid are problematic for two reasons. First, transcutaneous localization and intraoperative identification of SLNs is difficult, because SLN-to-background radioactivity ratios are low. Second, because of the variability in postinjection sulfur colloid migration times, use of operating room time may be inefficient. Because of the problems associated with same-day injections of radiolabeled colloid, we examined the utility of day-before-surgery injections of high-dose 99mTc-labeled sulfur colloid.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This study used patients who underwent SLN biopsy for breast cancer at the Nellie B. Connally Breast Center at The University of Texas M. D. Anderson Cancer Center between January and August of 2000. All patients had clinically negative axillae and biopsy-proven breast cancer and had given written informed consent for SLN biopsy. The patient information was entered prospectively into a database. The following parameters were recorded: tumor stage, tumor location, pathologic features of the primary tumor, prior procedures performed on the affected breast, type of drainage seen on the lymphoscintigram, dose and time of radioisotope injection, procedure performed at time of SLN biopsy, success or failure of attempted SLN identification, number of SLNs removed, character of each SLN (blue-stained or radioactive or both), disease status of each SLN (histologically positive or negative), and whether or not the patient had a completion axillary node dissection.

All patients underwent preoperative lymphoscintigraphy followed by intraoperative lymphatic mapping using a combination of 1% isosulfan blue dye and filtered 99mTc-labeled sulfur colloid. Patients whose operative procedure is done the same day as their colloid injection usually are given 0.5 mCi of 99mTc-labeled sulfur colloid. In this study, we wanted counts per second to be similar to or higher than counts with same-day injections. Because the half-life of 99mTc is 6 hours, we chose a dose of 2.5 mCi to account for the anticipated decay of 99mTc during overnight migration. The day before surgery, 2.5 mCi of 99mTc-labeled sulfur colloid (CIS-US, Bedford, MA) in a volume of 4 ml was injected in divided aliquots into the breast tissue surrounding the primary tumor or biopsy cavity. In the case of nonpalpable lesions, injections were performed under sonographic or mammographic guidance.

A lymphoscintigram was obtained after the sulfur colloid injection. Sulfur colloid injection and lymphoscintigraphy were done in the nuclear medicine department. On the day of surgery, 5 ml of 1% isosulfan blue dye (Lymphazurin, United States Surgical Corporation, Norwalk, CT) was injected around the tumor just prior to incision. A handheld gamma probe (neo 2000, Neoprobe Corporation, Dublin, OH) was used to identify the area in the axilla with the greatest activity in counts per second (the "hot spot"). A skin incision was made over the hot spot, and the surgeon searched for SLNs using the handheld gamma probe9,20 and the blue dye.10 A node was judged to be an SLN if it was blue-stained or had counts at least five times those of background radioactivity in vivo, or both. The biopsy site was examined after SLN removal to ensure that all radiolabeled lymph nodes and blue-stained lymph nodes were removed. The radioactivity of each node believed to be an SLN was measured ex vivo to ensure that the proper lymph node had been removed (i.e., to ensure that radioactivity was at least five times the background counts). The patient then underwent any further planned surgery on the primary breast tumor, either mastectomy or lumpectomy. While the patient was in the operating room, each SLN was evaluated using touch preparation techniques and, if the result on touch preparation evaluation was inconclusive, frozen section techniques. If an SLN was positive for metastatic disease on intraoperative evaluation, a complete axillary lymph node dissection was performed. A complete axillary dissection also was performed in patients in whom no SLN could be identified and when the surgeon had performed relatively few SLN biopsies and was trying to determine his or her own false-negative rate. If all the SLNs were negative for metastases on intraoperative evaluation, each SLN was embedded in paraffin and examined with hematoxylin and eosin staining of serial sections and immunohistochemical staining with anticytokeratin antibodies. Patients who had micrometastases detected on detailed examination of SLNs and who did not undergo completion axillary dissection were enrolled in ongoing clinical breast cancer trials at The M. D. Anderson Cancer Center.

We determined the proportion of patients in whom SLNs were identified on lymphoscintigraphy, the proportion of patients in whom SLNs were identified transcutaneously and intraoperatively, the methods of identification of SLNs (i.e., blue staining or high radioactivity or both), and the false-negative rate.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
We identified 117 patients who underwent SLN biopsy with day-before-surgery injection of high-dose 99mTc-labeled sulfur colloid between January and August 2000. Patient and tumor characteristics are presented in Table 1. Twenty-six patients received preoperative chemotherapy as a component of their treatment.


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  		TABLE 1. Patient demographics and tumor characteristics
 
The interval between radioisotope injection and SLN biopsy ranged from 15 to 20 hours. Lymphoscintigraphy showed drainage from the tumor in 107 (91%) of the 117 patients (Table 2). All patients with drainage visible on lymphoscintigraphy had drainage to the axilla, and 20% had drainage to the internal mammary nodes as well. No patients had drainage solely to the internal mammary nodes. An SLN was localized transcutaneously in 102 (95%) of the 107 patients with documented drainage on lymphoscintigraphy but in only 2 (20%) of the 10 patients without documented drainage. An SLN was identified intraoperatively in all of the patients who had documented drainage on lymphoscintigraphy but in only 7 (70%) of the 10 patients with no documented drainage. In 3 patients, no SLN was identified. Thus, the success rate for SLN mapping in this series was 114/117, or 97.5%.


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  		TABLE 2. Rate of transcutaneous localization and intraoperative identification of sentinel lymph node according to lymphoscintigraphy results
 
All three patients in whom mapping failed to identify an SLN had tumors in the upper outer quadrant of the breast. Two of the patients had invasive cancer (T1 and T2), and one had multicentric ductal carcinoma in situ. One patient had previously undergone an excisional biopsy, and two had previously undergone core biopsies. None of these three patients had received preoperative chemotherapy.

The mean number of counts per second (±SD) in the hot spot prior to excision was 645 ± 1014. The mean ratio of hot spot radioactivity to background radioactivity was 24 ± 41. The mean number of SLNs identified per patient was 2.3 (range, 1–8); the total number of SLNs removed was 266. The incidence of colocalization of the colloid and the blue dye was 72% for all SLNs harvested (Table 3). Colocalization was more frequent in SLNs that contained metastases (Table 3).


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  		TABLE 3. Method of identification and histologic assessment of SLNs
 
Twenty-five patients (21%) had at least one histologically positive SLN, and a total of 35 positive SLNs were identified among these 25 patients (Table 4). In 23 of these 25 patients, the SLN with the highest radioactive counts (the "hottest" node) contained metastasis, and in the remaining 2 patients the positive SLN was both blue-stained and hot, although not the hottest node. In all node-positive patients, metastatic disease was found in the first or second SLN harvested. All blue-stained positive SLNs were also radioactive.


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  		TABLE 4. Tumor and lymph node data for patients with positive SLNs
 
Of the 117 patients in this series, only 41 (35%) underwent completion axillary dissection. Seventeen of these patients had positive SLNs, and 24 had negative SLNs. One patient with a negative SLN had metastases in non-SLNs. This patient had a clinically negative axilla at presentation and received preoperative chemotherapy for a T2 primary breast tumor. Therefore, on the basis of data from the 41 patients who underwent completion axillary dissection, the sensitivity of this technique was 94% ([true-positive = 17]/[true-positive = 17 + false-negative = 1]), and the false-negative rate was 5.5% ([false negative = 1]/[true-positive = 17 + false-negative = 1]). This compares favorably with the false-negative rates published in recent reports using day-before-surgery radioactive colloid injections (Table 5).21,24–28


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  		TABLE 5. Selected published series using day-before-surgery injection technique
 
Finally, all 117 patients were taken to the operating room on the day of surgery without delays imposed by scheduled injections (in the nuclear medicine department) or delayed radioactive colloid migration times.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study, we found that injecting high-dose 99mTc-labeled sulfur colloid (2.5 mCi) the day before surgery resulted in high rates of both transcutaneous and intraoperative SLN identification in patients with breast cancer. We were able to localize the SLNs transcutaneously in 89% of the patients in our series, and we were able to identify the SLNs at surgery in 97.5% of the patients in our series. These rates are similar to those achieved by other researchers20 using day of-surgery injections of radiolabeled sulfur colloid. Likewise, ratios of SLN radioactivity to background radioactivity, rates of transcutaneous localizations of SLNs, and rates of intraoperative identification of SLNs achieved with the day-before-surgery injection technique appeared to be similar to outcomes previously achieved with the day-of-surgery injection technique.15–20 Finally, all patients who received high-dose day-before-surgery injections were brought to the operating room as scheduled without delays imposed by scheduled injection (in the nuclear medicine department) or delayed radioactive colloid migration times.

The optimal interval between radioisotope injection and SLN biopsy has not yet been determined. Most published studies have evaluated the use of radioisotope injections given the day of surgery. In these studies,15–20 intervals between injection time and biopsy ranged from 30 minutes to 8 hours, and rates of intraoperative SLN identification ranged from 92% to 98%. Rates of transcutaneous SLN localization are not clearly discussed in most of the published studies.17,19 A recent multicenter study reported a transcutaneous SLN localization rate of 93%.20 Winchester et al. evaluated day-before-surgery injection of 1 mCi of technetium-labeled filtered sulfur colloid in 100 patients. Overnight migration times ranged from 16 to 20 hours. Sentinel lymph nodes were identified in 97% of patients, and the mean number of SLNs harvested was 2.8.21 The overall false-negative rate could not be ascertained, because completion axillary dissections were not performed in all patients. A summary of selected published results using day-before surgery injection is presented in Table 5. 24–28 Recent data presented by Chua et al. at the 23rd Annual San Antonio Breast Cancer Symposium (December 2000) suggest that the optimal interval between injection time and surgery is between 20 and 300 minutes. They observed that false-negative rates tended to rise with time delays greater than 5 hours. However, the interval between injection time and surgery in our series was up to 20 hours, and the false-negative rate (in the evaluable patients) was 5.5%, which compares favorably with rates in other published series (Table 5).

Another concern about day-before-surgery radioisotope injection is that the time delay may promote significant passage of sulfur colloid to second-echelon nodes. Our data suggest the contrary; in our study, the delay of 15 to 20 hours between injection and surgery did not lead to an excess number of SLNs harvested (mean, 2.3) as compared to the number of SLNs harvested in studies of day-of-surgery injection (mean, 2.0) or day-before-surgery injection (Table 5). Furthermore, the facts that all metastases were found in the first or second SLN harvested and that all blue SLNs with metastases also were radioactive support the accuracy of this technique. Another important finding was that in 92% of patients with positive SLNs, the "hottest" SLN (the node with the highest counts per second) contained metastases. In both cases in which the SLN with metastases was not the hottest node, the SLN was both blue and hot.

In this study, we localized SLNs using a combination of day-before-surgery injection of high-dose 99mTc-labeled sulfur colloid, lymphoscintigraphy, and blue dye. Our success rate in identifying the SLN (97.5%) was similar to that in other studies using sulfur colloid and blue dye.12,13,16–19 A recent study concluded that preoperative lymphoscintigraphy does not improve the ability to identify the SLN during surgery and does not help lower false-negative rates.29 In our experience, the failure of lymphoscintigraphy to demonstrate drainage indicates a 20% chance of mapping failure (C. C. Solorzano, unpublished observations, 2001). Therefore, we continue to use lymphoscintigraphy, because it helps identify alternate patterns of drainage and helps us counsel patients regarding their risk of mapping failure when there is no apparent drainage. These patients can be prepared for a level I and II axillary dissection for appropriate staging.

Previous studies have established that the ability to identify the SLN improves with the experience of the surgeon. At our institution, all surgeons who perform SLN biopsy for breast cancer have performed at least 30 SLN biopsies using low-dose 99mTc-labeled sulfur colloid injected the day of surgery. It is likely that the accuracy of the current high-dose procedure will continue to improve and that the false-negative rate will decline. The one false-negative result observed in this series occurred early in the use of the technique and, in addition, occurred in a patient who had received preoperative chemotherapy.30 The acceptable false-negative rate for SLN biopsy in breast cancer has not yet been determined. Although the false-negative rate was based on a small number of patients with positive SLNs, the false-negative rate in this study compares favorably with that reported recently by Krag et al.20 and with the false-negative rates reported in other studies using the day-before-surgery injection technique (Table 5).21,24–28

In summary, day-before-surgery injection of high-dose 99mTc-labeled sulfur colloid (2.5 mCi) results in high rates of transcutaneous as well as intraoperative SLN localization. Furthermore, the false-negative rate observed using this technique is similar to that observed in studies using day-of-surgery radioisotope injection. Finally, the high-dose technique avoids delays imposed by day-of-surgery injection and allows efficient use of operating room time.


   Acknowledgments
 
The authors thank Stephanie Deming for her editorial assistance in preparing this manuscript.


   Footnotes
 
Presented at the 54th Annual Meeting of the Society of Surgical Oncology, Washington, DC, March 15-18, 2001.

Received for publication February 28, 2001. Accepted for publication August 16, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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