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Annals of Surgical Oncology 9:77-81 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Subareolar Injection of 99mTc Facilitates Sentinel Lymph Node Identification

Todd M. Tuttle, MD, Marybeth Colbert, MD, Robert Christensen, MD, Kevin J. Ose, MD, Thomas Jones, MD, Robert Wetherille, MD, Joel Friedman, MD, Karen Swenson, RN and Kelly M. McMasters, MD, PhD

From the Department of Surgery (TMT, MC, RC, KJO, TJ, RW, JF) and the Institute of Research and Education (KS), Park Nicollet Clinic, Minneapolis, Minnesota; the Department of Surgery (TMT), University of Minnesota, Minneapolis, Minnesota; and the Department of Surgery (KM), University of Louisville, Louisville, Kentucky.

Correspondence: Address correspondence and reprint requests to: Todd M. Tuttle, MD, Surgical Oncology, University of Minnesota, Mayo Mail Code 195, 420 Delaware St. SE, Minneapolis, MN 55455; Fax: 612-624-6969; E-mail: tuttl006{at}umn.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Sentinel lymph node (SLN) biopsy with the standard intraparenchymal injection has been accepted as an alternative to routine axillary dissection for patients with breast cancer. However, the identification and false-negative rates with this method can vary widely from surgeon to surgeon. The subareolar location contains a rich lymphatic network and represents a potential site of injection for SLN identification.

Methods: Between August 1, 1999, and December 31, 2000, we performed 159 SLN biopsy procedures on 158 patients with breast cancer. For each patient, 99mTc-labeled sulfur colloid was injected into the subareolar location, and 1% isosulfan blue dye was given as an intraparenchymal injection.

Results: In every case, at least one radioactive SLN was identified with the subareolar injection of technetium; a blue SLN was found in 97% of the cases. The blue SLN was also radioactive in 98% of the cases, indicating that the blue dye injected around the tumor and the technetium injected into the subareolar location drained to the same SLN.

Conclusions: Subareolar injection of technetium can improve SLN identification rates for breast cancer. The simplicity and accuracy of this technique may also reduce the variable results reported with the standard intraparenchymal method.

Key Words: Sentinel lymph node biopsy • Lymphatic mapping • Subareolar injection • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The status of the axillary lymph node basin is the most powerful predictor of long-term survival in patients with breast cancer. Pathologic analysis of the axillary nodes also provides essential information used to determine the administration of adjuvant therapies. Until recently, a level I/II axillary lymph node dissection was the standard surgical procedure to identify nodal metastases. However, axillary lymphadenectomy is associated with immediate and long-term side effects, including arm numbness and pain, fluid collections, infections, and lymphedema. Sentinel lymph node (SLN) biopsy has been proposed as a substitute for routine lymph node dissection in patients with clinically normal axillary lymph nodes. Several single-center and multicenter studies have documented the results of SLN biopsy followed by a planned axillary dissection.1–7 These studies have confirmed the hypothesis that the SLN is the first axillary node to receive lymphatic drainage from breast cancer. A recent multicenter study of 806 patients reported successful SLN identification in 88% of patients, with a false-negative rate of 7.2%.2

Although a number of different SLN identification techniques have been described, most published series have used a peritumoral or intraparenchymal injection of blue dye, technetium, or both. Unfortunately, the identification rate and accuracy of SLN biopsy can be quite variable with an intraparenchymal injection. In a multicenter validation trial with intraparenchymal injection of technetium, the false-negative rate varied from 0% to 28.6% depending on the surgeon.4 A contributing factor to the inconsistent results is that the lymphatic network deep in the breast parenchyma is often poor and unpredictable. Therefore, only a small fraction of the tracer injected into the mammary tissue actually reaches the axillary SLN, making identification more difficult. Given these difficulties, most investigators have reported a significant learning curve. In fact, a recent consensus statement from the American Society of Breast Surgeons recommends that surgeons perform at least 20 SLN biopsies before abandoning axillary dissection.8 Unfortunately, this recommendation is often not practical for surgeons treating patients outside a major breast center.

In contrast to the breast parenchyma, the subareolar location contains a rich lymphatic network that ultimately drains to the axilla.9 The subareolar location offers a potential alternative site for tracer injection to facilitate SLN identification for breast cancer. Klimberg et al.10 recently demonstrated that technetium injected into the subareolar location drained to the same SLN as blue dye injected around the breast tumor; the authors concluded that lymphatic drainage of the subareolar region mirrors that of the breast parenchyma. Kern,11 by use of a subareolar injection of blue dye alone followed by a planned axillary node dissection, identified a blue SLN in 39 of 40 patients; the SLN contained metastases in every patient with positive axillary lymph nodes. If these studies are confirmed, SLN biopsy may prove more practical and applicable to more surgeons treating breast cancer today. The purpose of this large single-institution study is to corroborate these reports with the subareolar injection technique.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
One hundred fifty-nine SLN biopsy procedures were performed on 158 patients with breast cancer from August 1, 1999, to December 31, 2000, at Park Nicollet Clinic, Minneapolis, MN. One patient had bilateral synchronous breast cancers and underwent bilateral SLN biopsy. Standard informed consent was obtained from each patient. All procedures were performed by one of seven surgeons with specific training and experience with SLN biopsy for breast cancer. Patients with biopsy-proven breast cancer, clinical stage T1N0 to T2N0, were eligible. Five patients included in our analysis were initially thought to have clinical T1 or T2 tumors but were found to have pathologic T3 tumors. Another patient included in our analysis had a needle biopsy of a nonpalpable tumor demonstrating ductal carcinoma in situ with possible microinvasion; however, on the final pathologic examination, no invasive disease was identified.

Technique
The SLN biopsy technique was performed in a standardized fashion. On the day of surgery, .75 mCi of filtered 99mTc-labeled sulfur colloid was injected with a 27-gauge needle. The needle entered the skin below the nipple at the 6:00 position, regardless of tumor location, and the technetium was injected into the subareolar location. For our first five patients, a total volume of 5 ml of technetium was injected. However, injection of this large volume was often painful, so we decreased the total volume to .5 ml for the rest of our patients, who experienced significantly less discomfort.

Lymphoscintigrams were not routinely obtained. From 1 to 4 hours after technetium injection and 10 minutes before the skin incision, 5 ml of 1% isosulfan blue (Lymphazurin; US Surgical Corporation, Norwalk, CT) was injected into the breast parenchyma surrounding the tumor in the operating room. For patients with intact, palpable tumors, the blue dye was injected at the 12:00, 3:00, 6:00, and 9:00 positions. For patients with intact, nonpalpable tumors, the blue dye was administered as a single injection adjacent to the tumor, by using radiographic guidance. For patients who had previous excisional biopsies, blue dye was injected around the biopsy cavity. A hand-held gamma probe (Neoprobe, Dublin, OH) was used to identify a transcutaneous hot spot, and then an axillary incision was made. The gamma probe guided the dissection to a blue-stained afferent lymphatic channel or blue-stained SLN.

All axillary lymph nodes with counts greater than or equal to 10% of the ex vivo counts of the most radioactive lymph node were removed and designated as SLNs. A blue node was defined as any lymph node staining blue or as any nonblue node connected to a clearly identified blue afferent lymphatic channel. After removing all blue and radioactive lymph nodes, the axilla was explored by digital examination to detect any grossly enlarged or hard lymph nodes. After removing all SLNs, we performed either a partial or total mastectomy.

Pathologic Examination
Pathologic examination was performed in a standardized fashion. Each SLN was analyzed with serial sectioning, with six levels of hematoxylin and eosin (H&E) stains plus two levels of immunohistochemistry for cytokeratin. SLNs were considered positive only if tumor cells could clearly be identified on H&E staining. SLNs containing scattered, individual cytokeratin-positive cells that were not clearly recognized as tumor cells on H&E were considered negative. If the SLN contained metastatic disease, a complete axillary lymph node dissection was usually performed.

Statistical Analysis
SLN identification rates for both the subareolar and intraparenchymal techniques were calculated and reported at 95% confidence intervals.12 The incidence of SLN metastases according to tumor stage was determined, and statistical trends were reported as previously described.13


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A total of 159 SLN biopsy procedures using the subareolar technique were performed on 158 patients with breast cancer. Table 1 lists the patient and tumor characteristics. Partial mastectomy was performed in 74% of cases and total mastectomy in 26%.


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  		TABLE 1. Clinical and pathological characteristics of the patient population
 
The mean number of SLNs removed per procedure was 1.8; the median was 2 (range, 1–5). At least 1 radioactive SLN was identified in all 159 procedures after subareolar technetium injection (Table 2). Because we did not routinely perform lymphoscintigraphy, we did not remove nonaxillary lymph nodes. With the peritumoral injection of blue dye, we found at least 1 blue SLN each in 154 cases (97%). However, the blue node was often found by dissection guided by the gamma probe. Of these 154 cases, the blue SLN was also radioactive in 151 (98%) procedures. In the three discordant cases, the technetium injected into the subareolar location drained to another axillary node that was not blue stained.


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  		TABLE 2. SLN identification
 
In 38 (24%) of the 159 procedures, the SLN contained metastatic disease. The incidence of positive SLNs by tumor size is shown in Table 3. No blue SLN was identified in five patients; metastases were found in radioactive SLNs in one of these five patients. It is important to note that metastatic disease was not identified in any of the three cases in which an SLN was blue, but not radioactive. After removal of all blue radioactive lymph nodes, we explored the axilla by digital examination. We identified two patients with hard, grossly enlarged, tumor-replaced axillary lymph nodes that were neither radioactive nor blue stained. In both of these patients, other blue, radioactive lymph nodes were removed and defined as SLNs but did not contain metastases. Completion axillary lymph node dissection was performed in 27 patients; additional positive nodes were identified in 13 (48%).


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  		TABLE 3. Incidence of SLN metastases by tumor stage
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
SLN biopsy is the most significant advancement in the surgical management of breast cancer since the establishment of breast conservation. This minimally invasive procedure can spare node-negative patients unnecessary axillary dissections and the subsequent complications. Numerous studies, with a collective sample of several thousand patients, have shown that that SLN biopsy can be performed with an acceptable false-negative rate by experienced surgeons.1–7 The vast majority of these studies have used an intraparenchymal (peritumoral) injection of technetium, blue dye, or both. However, the application of this procedure in general surgical practice continues to be limited by variable results and by a steep learning curve. Factors associated with either an inability to identify an SLN or a high false-negative rate include the following: previous excisional biopsy, advanced patient age, use of a single tracer agent, surgeon inexperience, and especially tumor location in the upper outer quadrant of the breast.1–4 Intraparenchymal injection of technetium around a tumor in the upper outer quadrant of the breast may result in shine-through, thus obscuring an axillary SLN that may be separated from the injection site by only a few centimeters.

A number of investigators have attempted to overcome the limitations of intraparenchymal injection by altering the technique. For instance, Veronesi et al.14 injected 99mTc-labeled human serum albumin into the subdermal location close to the breast tumor and identified an axillary SLN in 98% of patients, with a false-negative rate of only 5%. By use of a slightly different technique, Linehan et al.15 examined the results of intradermal injection of technetium. In their study, 100 patients received an intraparenchymal injection of blue dye and an intradermal injection of technetium. An SLN was found in all patients; the blue dye and technetium mapped the same SLN in 95% of patients. The authors concluded that the dermal and parenchymal lymphatics drain to the same SLN in most patients.

The subareolar lymphatic plexus has recently been examined as a site of tracer injection for SLN identification. Klimberg et al.10 injected 1.0 mCi (4 ml) of unfiltered technetium sulfur colloid into the subareolar area and 2 to 5 ml of isosulfan blue around the tumor. A blue SLN was identified in 62 of 69 cases, and all blue SLNs were also radioactive. In our study, we injected a similar dose (.75 mCi) of filtered technetium in a much smaller volume (.5 ml) into the subareolar location, in addition to injecting blue dye around the tumor. At least one radioactive SLN was found in all cases, and at least one blue SLN was found in 97% of procedures. However, the blue node was often found because the gamma probe directed the dissection to the radioactive blue SLN. The subareolar technetium injection technique facilitated the identification of blue nodes that may have otherwise been difficult or impossible to identify in the axilla. The blue SLN was also radioactive in 98% of patients, indicating that the peritumural and subareolar lymphatics drain to the same SLN. The average number of SLNs per patient (1.8) identified with our approach is similar to the published data from studies using intraparenchymal injection only.

The accuracy of the subareolar technique, as reported by Klimberg et al.10 and in this study, was not validated by a completion lymphadenectomy; rather, the results were correlated with the standard intraparenchymal injection of blue dye to determine whether the two agents actually mapped to the same SLN. As part of a multicenter study mandating completion lymphadenectomy, we previously demonstrated that intraparenchymal tracer injection has a low false-negative rate at our institution.2 Thus, the analysis of the data presented here is a comparison with that validated technique. Moreover, in our series, the percentage of patients with positive SLNs according to T stage is consistent with other reports.1,2 In a study that included a planned axillary dissection, Kern11 injected blue dye only into the subareolar location and identified a blue SLN in 39 of 40 patients. Axillary metastases were found in 15 patients, and the SLN contained metastatic disease in all cases, with no false negatives. In the University of Louisville Breast Cancer Sentinel Lymph Node Study, 85 cases of subareolar injection have been performed, with a false-negative rate of only 5.9%.16 In our series of 159 procedures, no patient had blue-stained, nonradioactive SLNs containing metastatic disease. However, the true false-negative rate in this study is not known because we did not perform axillary lymph node dissection if the SLN biopsy was negative. We observed two patients who had palpable tumor-replaced non-SLNs without metastases in blue, radioactive SLNs. Others have reported similar findings, which suggest that bulky metastatic tumor in the true SLN or in the afferent lymphatic channel may actually divert injected tracer agents to blue, radioactive lymph nodes that do not contain metastases.17 A digital examination of the axilla is therefore mandatory after removal of all blue and radioactive lymph nodes, regardless of the injection technique used.

This study contributes to a growing body of evidence supporting the theory that tumors of the breast, regardless of location, drain through a common afferent lymphatic channel to a common axillary SLN. This model would explain the successful localization of breast SLN biopsy with any of the reported techniques, including intraparenchymal, subdermal, intradermal, and subareolar injection. In 1963, Halsell et al.9 demonstrated that contrast media injected directly through a lymphatic channel into the periareolar area drained to the intramammary lymphatics and subsequently to the axilla. Using a subareolar injection of blue dye, Kern11 described a constant "sentinel lymphatic channel" exiting the breast over the lateral edge of the pectoral major muscle and entering the axilla. These studies suggest that the lymphatic drainage of the breast should be considered as a unit, thus making the subareolar location ideal for SLN injection.

In our series, we did not routinely perform preoperative breast lymphoscintigraphy. Previously, investigators have demonstrated that an intraparenchymal injection of technetium results in a low SLN identification rate on preoperative lymphoscintograms.3,4 Even if an SLN is not identified on preoperative imaging, a radioactive SLN is still usually found with surgical exploration using a gamma probe. A multicenter trial found that preoperative lymphoscintigraphy did not improve SLN identification, nor did it reduce the false-negative rate, but it did significantly increase the cost.3 One argument against subareolar injection without preoperative lymphoscintigraphy is that internal mammary SLNs would not be identified. In a small series of 30 patients who underwent preoperative lymphoscintigraphy after subareolar injection of technetium, no extra-axillary SLN was found.18 Even if internal mammary lymph nodes are identified on preoperative lymphoscintigraphy, the incidence of isolated internal mammary metastases in the absence of axillary metastases is low.19 Therefore, we do not believe that routine preoperative lymphoscintigraphy is necessary for SLN identification.

The subareolar location offers a number of potential advantages over the standard intraparenchymal injection around the breast tumor. First, this approach is easy, requires less expertise, and eliminates the need for image-guided injection for nonpalpable tumors. In contrast to the intramammary tissue, a rich lymphatic network is located beneath the areola; as a result, a higher percentage of the injected tracer agent reaches the SLN, making identification much easier and decreasing the learning curve. Second, after an intraparenchymal injection, the patient and surgeon may have to wait several hours for technetium to reach the SLN. However, a recent report has demonstrated that technetium reaches the axilla within a few minutes after subareolar injection, thereby making surgery schedules much more predictable.15 We are investigating the utility of an intraoperative subareolar injection of technetium to avoid patient discomfort and delays in surgery. Third, the subareolar injection increases the distance between the injection site and the axillary SLN, thus reducing the shine-through effect from tumors located in the upper outer location of the breast. Finally, if the common lymphatic channel theory is confirmed, SLN biopsy with the subareolar approach may be indicated for patients with multifocal breast cancer. We believe that the simplicity and accuracy of subareolar injection should make SLN biopsy more applicable for general surgeons treating breast cancer patients.


   Acknowledgments
 
The authors thank Mary Knatterud for her editorial assistance with this manuscript and Professor Chap Le for his statistical analysis of all results.

Received for publication March 8, 2001. Accepted for publication August 24, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Martin RCII, Edwards MJ, Wong SL, et al. Practical guidelines for optimal gamma probe detection of sentinel lymph nodes in breast cancer: results of a multi-institutional study. Surgery 2000; 128: 139–44.[CrossRef][Medline]
  2. McMasters KM, Tuttle TM, Carlson DJ, et al. Sentinel lymph node biopsy for breast cancer: a suitable alternative to routine axillary dissection in multi-institutional practice when optimal technique is used. J Clin Oncol 2000; 18: 2560–6.[Abstract/Free Full Text]
  3. McMasters KM, Wong SL, Tuttle TM, et al. Preoperative lymphoscintigraphy for breast cancer does not improve the ability to identify sentinel lymph nodes. Ann Surg 2000; 231: 724–31.[CrossRef][Medline]
  4. Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer—a multicenter validation study. N Engl J Med 1998; 339: 941–6.[Abstract/Free Full Text]
  5. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220: 391–401.[Medline]
  6. Krag DN, Weaver DL, Alex JC, Fairbank JT. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 1993; 2: 335–40.[CrossRef][Medline]
  7. Albertini JJ, Lyman GH, Cox C, et al. Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA 1996; 276: 1818–22.[Abstract]
  8. Edwards MJ, Giuliano A, Reintgen D, et al. Consensus statement on sentinel lymph node biopsy: guidelines for performance of sentinel lymph node biopsy for breast cancer. American Society of Breast Surgeons. 2000. Available at: http://www.breastsurgeons.org/sentinel.htm. Accessed October 30, 2001.
  9. Halsell J, Smith J, Bentlage C, Park O, Humphreys J. Lymphatic drainage of the breast demonstrated by vital dye staining and radiography. Ann Surg 1963; 162: 221–6.
  10. Klimberg V, Rubio I, Henry R, Cowan C, Colvert M, Korourian S. Subareolar versus peritumoral injection for location of the sentinel lymph node. Ann Surg 1999; 229: 860–5.[CrossRef][Medline]
  11. Kern K. Sentinel lymph node mapping in breast cancer using subareolar injection of blue dye. J Am Coll Surg 1999; 189: 539–45.[CrossRef][Medline]
  12. Louis TA. Confidence intervals for a binomial parameter after observing no successes. Am Stat 1981; 35: 154.
  13. Le CT, Boen JR. Health and Numbers: Basic Biostatistical Methods. New York: Wiley, 1995: 202–204.
  14. Veronesi U, Paganelli G, Galimberti V, et al. Sentinel node biopsy to avoid axillary dissection in breast cancer with clinically negative nodes. Lancet 1997; 349: 1864–7.[CrossRef][Medline]
  15. Linehan D, Hill A, Akhurst T, et al. Intradermal radiocolloid and intraparenchymal blue dye injection optimize sentinel node identification in breast cancer patients. Ann Surg Oncol 1999; 6: 450–4.[Abstract]
  16. McMasters KM, Wong SL, Martin RC, et al. Dermal injection of radioactive colloid is superior to peritumoral injection for breast cancer sentinel lymph node biopsy: results of a multiinstitutional study. Ann Surg 2001; 233: 676–87.[CrossRef][Medline]
  17. Borgstein PJ, Meijer S, Pijpers R, Van Diest PJ. Functional lymphatic anatomy for sentinel node biopsy in breast cancer: echoes from the past and the periareolar blue method. Ann Surg 2000; 232: 81–9.[CrossRef][Medline]
  18. Kern KA, Rosenberg RJ. Preoperative lymphoscintigraphy during lymphatic mapping for breast cancer: improved sentinel node imaging using subareolar injection of technetium 99m sulfur colloid. J Am Coll Surg 2000; 191: 479–89.[CrossRef][Medline]
  19. Morrow M, Foster RS. Staging of breast cancer: a new rationale for internal mammary node biopsy. Arch Surg 1981; 116: 748–51.[Abstract]



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