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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:20-24 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Intradermal Isotope Injection: A Highly Accurate Method of Lymphatic Mapping in Breast Carcinoma

Susan K. Boolbol, MD, Jane V. Fey, MPH, Patrick I. Borgen, MD, Alexandra S. Heerdt, MD, MPH, Leslie L. Montgomery, MD, Michael Paglia, MD, Jeanne A. Petrek, MD, Hiram S. Cody III, MD and Kimberly J. Van Zee, MS, MD, FACS

From the Breast Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence to: Dr. Kimberly J. Van Zee, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, MRI 1026, New York, NY 10021; Fax: 212-794-5812.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
BACKGROUND: The combined approach of radioactive tracer and blue-dye mapping of sentinel lymph nodes (SLN) has evolved into a safe and effective alternative to routine axillary node dissection in specific patient populations with breast carcinoma. The optimal route of injection for the isotope has not been clearly defined. To assess the intradermal route of isotope injection, we prospectively evaluated 100 patients with biopsy-proven invasive breast carcinoma with SLN biopsy followed by planned axillary node dissection.

METHODS: All patients were given an intradermal injection of Tc-99m sulfur colloid and an intraparenchymal injection of blue dye. All patients underwent a complete axillary node dissection. Each sentinel node was serially sectioned and examined by immunohistochemistry.

RESULTS: Sentinel nodes were successfully identified in 99% of cases. Forty-six patients had axillary metastases; of these, four had falsely negative sentinel nodes (false-negative rate, 9%). The false-negative rate was 0 of 24 (0%) for T1 tumors, 2 of 18 (11%) for T2 tumors, and 2 of 4 (50%) for T3 tumors. Three of four patients with false negatives had palpable, clinically suspicious axillary nodes found intraoperatively. If these cases are excluded, the accuracy of the procedure was 100% for T1 and T2 tumors. Of the 42 positive axillae identified by SLNB (true positives), 40 were localized using the intradermal injection of radioisotope; in 13 of these cases, this was the only method that identified the true-positive node.

CONCLUSION: These data demonstrate that intradermal injection of radioactive tracer is an effective method of localizing the SLN in cases involving small breast cancers. Further investigation is warranted before this technique is adopted for use in larger breast cancers. Intraoperative examination and biopsy of any suspicious nonsentinel nodes are critical.

Key Words: Sentinel lymph node biopsy— • Breast carcinoma— • Intradermal isotope— • Intraparenchymal isotope— • Lymphatic mapping.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Axillary lymph node status remains the single most important prognostic indicator in patients with invasive breast carcinoma. Historically, axillary lymph node dissection has provided this critical staging information. Due to heightened public awareness and increasingly widespread use of screening mammography, as well as to significant improvements in mammographic quality and sensitivity, the proportion of women with breast cancer diagnosed at Stages 0 and I has increased markedly in recent decades. Thus, an increasing number of women may benefit from a more selective approach to the axilla. The sentinel lymph node biopsy (SLNB) technique has the potential to decrease the surgical morbidity of axillary node dissection while still providing essential staging information.

The phrase "sentinel node" first appeared in 1960 in a paper by Gould et al.1 in reference to cancer of the parotid gland. Cabanas,2 apparently unaware of the previous report, used this phrase in 1977 for the staging of penile cancer. He showed that lymphatic mapping could be used to identify the regional node most likely to be the first site of metastatic disease, terming this the "sentinel node." In 1992, Morton and associates3 demonstrated the validity of this technique in melanoma. Shortly thereafter, several groups,4–7 using a variety of lymphatic mapping techniques, extended this methodology to patients with early-stage breast carcinoma.

Krag4 pioneered the use of radiolocalization of the sentinel lymph node in breast carcinoma, and Giuliano5 was the first to apply lymphatic mapping to breast cancer using blue dye alone. A combination of radiolocalization and blue-dye mapping, first reported by Albertini,6 was shown to shorten the learning curve for the procedure and to further increase its accuracy. Others have reported modifications of these techniques: intradermal injection of blue dye8 or injection of blue dye into the subareolar plexus,9 subdermal injection of radioisotope,10 or subareolar injection of radioisotope and peritumoral injection of blue dye.11 Controversy exists regarding the optimal method of localizing the sentinel node.

Our institution’s early experience with lymphatic mapping, utilizing both intraparenchymal blue dye and intraparenchymal radioisotope injection, demonstrated a 93% success rate (number of patients who had a SLN identified/number of patients who had an attempted SLNB) with a 95% accuracy rate7 ([number of patients with true-positive SLNs + number of patients with true-negative SLNs]/total number of patients in whom a SLN was identified). Subsequently, in a series of 200 patients, SLNB was performed with intraparenchymal blue dye and either intraparenchymal or intradermal radioisotope injection.12 This study demonstrated a high degree of concordance between the blue dye and the radioisotope, regardless of the site of radioisotope injection, suggesting that an intradermal injection results in accurate localization of the SLN. In this study, radioisotopic sentinel lymph node localization was successful in 78% of cases with intraparenchymal injection and in 97% of those with intradermal injection, a statistically significant difference (P < .001).12 In the present study, we assessed the accuracy and false-negative rates of the combined used of intradermal radioisotope injection and intraparenchymal blue-dye injection in a series of 100 patients with breast carcinoma who underwent SLNB followed by planned completion axillary dissection.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
One hundred and one consecutive patients undergoing lymphatic mapping and planned axillary node dissection were prospectively studied. Each of these patients had a biopsy-proven invasive breast carcinoma and a clinically node-negative axilla. In 100 of these patients, the SLNB procedure was successful (an SLN was identified by blue dye and/or isotope); these 100 patients constitute our patient population. Using AJCC staging criteria, there were 62, 34, and 4 patients with T1, T2, and T3 tumors, respectively.

Two to 4 hours before surgery, patients underwent intradermal injection of 0.1 mCi Tc-99 unfiltered sulfur colloid (0.05 ml) at a single site just superficial to the primary tumor location. In patients who had had a prior excisional biopsy, the injection was made in superolateral proximity to the prior incision. Lymphoscintigraphy was performed 50 to 60 minutes after injection. Counts were taken in the operating room of the room background, the injection site, and the "hot spot" in the axilla using a gamma probe. Approximately 10 minutes prior to skin incision, 1 to 5 ml of isosulfan blue (Lymphazurin; Zenith Parenterals, Rosemont, IL) were injected into the breast parenchyma surrounding the tumor or near the biopsy cavity.

The axillary skin incision was made over the area of greatest activity noted in counts per second. Careful dissection was used to identify the blue-stained lymphatic channels leading to the blue-stained node. The gamma probe was used intraoperatively to help guide the dissection. Successful blue-dye localization was defined as localization of a lymph node with visible blue staining, a directly contiguous blue-stained afferent lymphatic, or both. Successful identification of the sentinel node by radiolocalization was defined as a ratio of ex vivo SLN counts to postexcision axillary-bed counts of four or more to one, which corresponded well to the surgeon’s subjective impression of the success of the radiolocalization.

Following excision of the sentinel node, an axillary node dissection took place, during which a minimum of eight nodes was removed. All nodes were bisected and routinely examined following staining with hematoxylin and eosin (H&E). In addition, all sentinel nodes found to be negative by routine examination were subsequently serially sectioned and stained for cytokeratin with CAM 5.2 (Becton Dickinson) and AE1:AE3 (Boehringer Mannheim).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient and tumor characteristics are detailed in Table 1. The mean patient age was 54 years (range, 26 to 86 years). Fifty-five patients (55%) had had a previous surgical biopsy. Tumors were located in the upper-outer quadrant (56%), the lower-outer quadrant (7%), the upper-inner quadrant (21%), the lower-inner quadrant (2%), and centrally (14%). The lymphoscintigram was positive in 72% of patients. The majority of the tumors (85%) were invasive ductal carcinomas. Invasive lobular carcinomas accounted for 11% of cases, and 4% were medullary, colloid, or tubular carcinomas. Lymphovascular invasion was found in 38% of tumors. The minimum number of lymph nodes excised was 8, with a range of 8 to 47 nodes, a median of 16.5 nodes, and a mean of 17.6 nodes.


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  		Table 1. Patient and tumor characteristics
 
A sentinel node was successfully identified by blue dye alone in 7% of patients, by isotope alone in 15%, and by both blue dye and isotope in 78%. Of the 42 positive axillae identified by SLNB (true positives), 40 were localized utilizing the intradermal injection of radioisotope, and in 13 of these cases, this was the only method that identified the true-positive lymph node. Axillary nodal metastases were found in 24 of the 62 T1 cases (39%), in 18 of the 34 T2 cases (53%), and in each of the four T3 cases (100%) ( Table 2). The SLN correctly predicted the axillary status in 24 of 24 T1 cases (100%), in 16 of 18 T2 cases (94%), and in 2 of 4 (50%) T3 cases.


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  		Table 2. False-negative and accuracy rates of sentinel lymph node biopsy using intradermal isotope and peritumoral blue-dye injection, by tumor size
 
Of the total 46 patients with axillary metastases, SLNB identified 42, resulting in an overall accuracy rate of 96%. The false negatives were two T2 tumors and two T3 tumors and are described in Table 3. Three of the four patients with false-negative nodes had clinically suspicious nodes found during intraoperative dissection of the sentinel lymph node. In three of the four patients with false-negative nodes, the lymphoscintigram was negative.


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  		Table 3. Patients with falsely negative sentinel lymph nodes (n = 4)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Lymphatic mapping with sentinel lymph node biopsy is being adopted rapidly in the treatment of breast carcinoma as a less morbid method of staging the axilla than standard axillary lymph node dissection. The optimal technique, however, has not been defined. Here we have evaluated the accuracy and false-negative rates of lymphatic mapping using an intraparenchymal blue-dye injection and an intradermal isotope injection.

In Giuliano’s5 initial study using intraparenchymal injection of blue dye, an SLNB success rate of 66% with an accuracy rate of 96% was reported. Subsequent studies13,14 by that group and by others also using this technique have reported success rates ranging from 71% to 94% and accuracy rates between 97% and 100% ( Table 4). Krag et al.4 employed an intraparenchymal injection of radioisotope to achieve a SLNB success rate of 82% with 100% accuracy. Albertini et al.6 achieved a success rate of 92% with 100% accuracy using a combination of blue dye and radioisotope in a series of 62 patients. Veronesi and colleagues10 used a subdermal injection of isotope in 163 patients; SLNB was successfully performed in 98% of these patients, with 98% accuracy.


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  		Table 4. Sentinel lymph node biopsy series
 
The initial experience at the Memorial Sloan-Kettering Cancer Center used a combination of these two techniques, an intraparenchymal blue-dye injection with an intraparenchymal radioisotope injection, and resulted in a success rate of 93% and an accuracy rate of 95%.7 Linehan et al.12 later compared two consecutive series of 100 patients undergoing SLNB. The first group underwent SLNB using intraparenchymal injection of both isotope and blue dye; the second group had intradermal injection of radioisotope and intraparenchymal injection of blue dye. They found success rates of 92% and 100%, respectively, and concluded intradermal isotope injection was preferable due to its greater ease of injection and higher rate of success. In this study, we evaluated the accuracy of this technique in 100 patients undergoing SLNB with intradermal isotope and intraparenchymal blue-dye injection through planned axillary dissection.

There are several advantages to the intradermal route of injection. Patients report less pain with intradermal injection, and it requires less expertise, allowing nonphysicians to perform the injection. An intradermal injection also prevents inadvertent injection into the prior biopsy cavity. In addition, this route requires a smaller dose of isotope, resulting in lower counts at the injection site and less interference from the "blast" zone, thus allowing for a more precise use of radiolocalization in the axilla.

Embryologically, the breast develops from the ectoderm. The network of lymphatics communicates with the subdermal plexus15 and tends to drain into the axillary nodes.16 Borgstein et al.8 demonstrated 100% concordance in localizing the sentinel node using an intradermal injection of blue dye and an intraparenchymal injection of radioisotope. This high rate of concordance not only supported the theory that the intraparenchymal lymphatics drain into the same nodal basin as the lymphatics of the overlying skin; it showed that the two regions drain to the same sentinel node. Additional supporting evidence for this theory was provided by Linehan et al.,12 who reported a 95% concordance between intradermal radioisotope injection and intraparenchymal injection of blue dye. Klimberg et al.11 found a 95% concordance with subareolar injection of isotope and peritumoral blue dye. Using subareolar injection of blue dye alone, Kern9 achieved a success rate of 98% and an accuracy rate of 100%. These studies all suggest that, regardless of tumor location within the breast, all lymphatics drain to the same sentinel node.

Among our patients with T1, T2, and T3 carcinomas, we found an overall accuracy rate of 96%, a rate comparable to that of other published series (Table 4). If the four T3 cases are excluded, the accuracy rate rises to 98%; if the T1 cases alone are included, the accuracy is 100%.

Examination of the four cases in which the SLNB was falsely negative reveals that three of these four patients had obviously suspicious disease evident during intraoperative dissection of the SLN. If cases with intraoperative gross disease are eliminated, the accuracy rate of this technique is 100% for T1 and T2 tumors. In those cases of grossly involved nodes, the nodes had been replaced with tumor; it can be postulated that in such cases the lymphatic flow through the node has been obstructed. This observation also illustrates the importance of intraoperative examination of the axilla during SLN dissection. Examination of the axilla and removal of any suspicious lymph nodes should be considered essential components of this procedure.

The false-negative rate of 50% in T3 tumors suggests that this technique should not be adopted for cases involving larger tumors. Larger tumors have not only a greater likelihood of nodal metastasis, but also a greater likelihood of extensive nodal disease resulting in altered lymphatic drainage patterns.

In conclusion, intradermal injection is a highly accurate method of isotope delivery for lymphatic mapping of the breast and may, in fact, be preferable to intraparenchymal injection due to its greater ease of use and its higher rate of success.


   Footnotes
 
Presented at the 53rd Annual Meeting of the Society of Surgical Oncology, New Orleans, Louisiana, March 16–19, 2000.

Received for publication March 30, 2000. Accepted for publication August 8, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  7. O’Hea BJ, Hill ADK, El-Shirbany AM, et al. Sentinel lymph node biopsy in breast cancer: initial experience at Memorial Sloan-Kettering Cancer Center. J Am Coll Surg 1998; 186: 423–7.[CrossRef][Medline]
  8. Borgstein PJ, Meijer S, Pijpers R. Intradermal blue dye to identify sentinel lymph node in breast cancer. Lancet 1997; 349: 1668–9.[Medline]
  9. Kern KA. Sentinel lymph node mapping in breast cancer using subareolar injection of blue dye. J Am Coll Surg 1999; 189: 539–45.[CrossRef][Medline]
  10. Veronesi U, Paganelli G, Galimberti V, et al. Sentinel node biopsy to avoid axillary node dissection in breast cancer with clinically negative lymph nodes. Lancet 1997; 349: 1864–7.[CrossRef][Medline]
  11. Klimberg VS, Rubid IT, Henry R, et al. Subareolar versus peritumoral injection for location of the sentinel lymph node. Ann Surg 1999; 229: 860–4.[CrossRef][Medline]
  12. Linehan DC, Hill ADK, 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]
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  15. Grant RN, Tabah EJ, Adair FE. The surgical significance of the subareolar plexus in the cancer of the breast. Surgery 1959; 33: 71–8.
  16. Turner-Warnick RT. The lymphatics of the breast. Br J Surg 1959; 46: 574–82.[Medline]
  17. Pijpers R, Meijer S, Hoekstra OS, et al. Impact of lymphoscintigraphy on sentinel node identification with technetium 99m colloidal albumin in breast cancer. J Nucl Med 1997; 38: 366–8.[Abstract/Free Full Text]
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