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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:192-197 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Sentinel Lymph Node Biopsy for Melanoma: How Many Radioactive Nodes Should be Removed?

Kelly M. McMasters, MD, PhD, Douglas S. Reintgen, MD, Merrick I. Ross, MD, Sandra L. Wong, MD, Jeffrey E. Gershenwald, MD, David N. Krag, MD, R. Dirk Noyes, MD, Vicki Viar, RN, MSN, Patricia B. Cerrito, PhD and Michael J. Edwards, MD

From the Division of Surgical Oncology, Department of Surgery, James Graham Brown Cancer Center (KMM, MJE, SLW, and VV), and Department of Mathematics (PBC), University of Louisville, Louisville, Kentucky; University of South Florida, Moffitt Cancer Center, Tampa, Florida (DSR); University of Texas M.D. Anderson Cancer Center, Houston, Texas (MIR, JEG); Department of Surgery, University of Vermont, Burlington, Vermont (DNK); and LDS Hospital, Salt Lake City, Utah (RDN).

Correspondence: Address correspondence and reprint requests to: Dr. Kelly M. McMasters, University of Louisville-Brown Cancer Center, 529 S. Jackson St., Louisville, KY 40202; Fax: 502-852-8031; Email: kelly.mcmasters{at}nortonhealthcare.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Sentinel lymph node (SLN) biopsy has become a standard method of staging patients with cutaneous melanoma. Sentinel lymph node biopsy usually is performed by intradermal injection of a vital blue dye (isosulfan blue) plus radioactive colloid (technetium sulfur colloid) around the site of the tumor. Intraoperative gamma probe detection has been shown to improve the rate of SLN identification compared to the use of blue dye alone. However, multiple sentinel nodes often are detected using the gamma probe. It is not clear whether these additional lymph nodes represent true sentinel nodes, or second-echelon lymph nodes that have received radiocolloid particles that have passed through the true sentinel node. This analysis was performed to determine the frequency with which these less radioactive lymph nodes contain metastatic disease when the most radioactive, or "hottest," node does not.

Materials and Methods: In the Sunbelt Melanoma Trial, 1184 patients with cutaneous melanoma of Breslow thickness 1.0 mm or more had sentinel lymph nodes identified. Sentinel lymph node biopsy was performed by injection of technetium sulfur colloid plus isosulfan blue dye in 99% of cases. Intraoperative determination of the degree of radioactivity of sentinel nodes (ex vivo) was measured, as well as the degree of blue dye staining.

Results: Sentinel nodes were identified in 1373 nodal basins in 1184 patients. A total of 288 of 1184 patients (24.3%) were found to have sentinel node metastases detected by histology or immunohistochemistry. Nodal metastases were detected in 306 nodal basins in these 288 patients. There were 175 nodal basins from 170 patients in which at least one positive sentinel node was found and more than one sentinel node was harvested. Blue dye staining was found in 86.3% of the histologically positive sentinel nodes and 66.4% of the negative sentinel nodes. In 40 of 306 positive nodal basins (13.1%), the most radioactive sentinel node was negative for tumor when another, less radioactive, sentinel node was positive for tumor. In 20 of 40 cases (50%), the less radioactive positive sentinel node contained 50% or less of the radioactive count of the hottest lymph node. The cervical lymph node basin was associated with an increased likelihood of finding a positive sentinel node other than the hottest node.

Conclusions: If only the most radioactive sentinel node in each basin had been removed, 13.1% of the nodal basins with positive sentinel nodes would have been missed. It is recommended that all blue lymph nodes and all nodes that measure 10% or higher of the ex vivo radioactive count of the hottest sentinel node should be harvested for optimal detection of nodal metastases.

Key Words: Melanoma • Sentinel lymph node • Lymph node dissection • Lymphoscintigraphy • Lymphatic mapping


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Since the first report by Morton and colleagues in 1992,1 sentinel lymph node (SLN) biopsy has become a widely accepted method of staging regional lymph nodes for patients with melanoma. Sentinel lymph node biopsy is performed by intradermal injection of a vital blue dye (isosulfan blue), a radioactive tracer (technetium sulfur colloid), or both around the melanoma site. The sentinel node is then identified by use of an intraoperative hand-held Gamma counter and by visualization of the blue dye in an afferent lymphatic channel entering the blue-stained sentinel node. It has been demonstrated that the use of the blue dye in combination with the radioactive colloid leads to optimal detection and identification of sentinel nodes for melanoma.2–9

There is, however, some controversy about the exact definition of a sentinel node. It has been suggested that the blue dye staining of the afferent lymphatic channel leading into the sentinel node is the sine qua non of a true sentinel node, because it indicates a direct lymphatic pathway from the site of the melanoma.10,11 It is clear, however, that radioactive colloid injection with gamma probe detection often identifies sentinel nodes that would not have been detected with blue dye alone, and positive sentinel nodes that have no evidence of blue dye staining occasionally are identified.2–9

Several different definitions of the term sentinel node have been proposed based on the degree of radioactivity within the node. Among these are definitions based on the absolute number of counts in the node, or on the ratio of the in vivo or ex vivo radioactive counts in the node to background radioactivity or to neighboring non-sentinel nodes.10,11 All of these definitions are somewhat arbitrary, and none is based on empiric data related to the likelihood of finding nodal metastases. For example, the degree of background radioactivity is variable based on the position of the gamma probe within the nodal basin and the location of the primary tumor, which can account for a significant amount of background radioactivity, or "shine-through." Furthermore, the absolute number of counts in the node varies depending on the dose and type of radioactive colloid, the injection site, time interval from injection to operation, the type of gamma probe and its calibration, as well as other factors.

The present study was designed to address these issues using empiric data derived from the Sunbelt Melanoma Trial, a large multi-institutional trial of SLN biopsy and adjuvant therapy for melanoma. The results of this study indicate that the most radioactive, or "hottest," lymph node is not always the positive sentinel node, and that it is important to search diligently for additional sentinel nodes, especially if significant residual radioactive background remains after the first sentinel node is removed. Blue dye staining is usually, but not always, evident in the positive sentinel node.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients were enrolled in the Sunbelt Melanoma Trial, a randomized prospective trial involving 60 institutions across the United States, between June 1997 and January 2000. The study was approved at the institutional review boards of each center. Patients with cutaneous melanomas of Breslow thickness 1.0 mm or more and clinically negative regional lymph nodes were eligible. After informed consent was obtained, patients underwent SLN biopsy, during which time intraoperative determination of blue dye staining and degree of radioactivity of each sentinel node (ex vivo count) was determined. The protocol specified that all blue nodes, and all nodes containing 10% or more of the radioactive counts of the ex vivo count of the hottest node should be removed and designated SLN. These guidelines have been suggested previously.11,12 This analysis includes all patients in whom at least one SLN was identified, and for whom complete data were available regarding blue dye staining, histology, and radioactive counts in the sentinel nodes.

Blue dye staining in each sentinel node was graded as either none, faint blue, or obviously blue. Analysis was performed of patients with more than one sentinel node removed per nodal basin to determine how frequently the less radioactive sentinel nodes were positive for metastatic tumor. All sentinel nodes underwent histologic analysis with hematoxylin and eosin (H&E) staining at multiple levels followed by immunohistochemical staining for S100 protein. Sentinel nodes were divided into blocks based on lymph node size. At least five sections per block were evaluated by H&E staining and two sections per block by immunohistochemical staining for S100. Immunohistochemical staining for HMB-45 or MART-1 was performed at some institutions as well.

Lymphatic drainage to the following nodal basins was recorded: axilla, cervical (including supraclavicular and parotid), inguinal, deep groin (iliac, hypogastric, and obturator), epitrochlear, popliteal, and ectopic.

Statistical analysis was performed by {chi}2 analysis and Fisher’s exact test using the SAS (SAS Institute, Cary, NC) software package. Significance was determined at P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Clinicopathologic characteristics of patients entered into the study are presented in Table 1. There were 687 men and 497 women. Median age was 51 years. There were 1373 nodal basins in 1184 patients (mean, 1.12 basins/patient). A total of 2863 sentinel nodes were identified in 1373 basins (mean, 2.08 SLN/basin). Mean and median tumor thicknesses were 2.35 mm and 1.73 mm, respectively.


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  		TABLE 1. Clinicopathologic features of patient population
 
Blue dye injection in combination with radioactive colloid was used in 99% of cases. Sentinel nodes were identified in 99.7% of patients. A total of 288 of 1184 patients (24.3%) had histologic or immunohistochemical evidence of metastatic disease in the sentinel nodes. Nodal metastases were detected in 306 nodal basins in these 288 patients. To determine how often a less radioactive sentinel node is positive for tumor when the most radioactive lymph node is not, 175 positive nodal basins from 170 patients were identified in which more than one sentinel node was identified. In 40 of these 175 nodal basins, a less radioactive lymph node was positive for tumor when the most radioactive sentinel node was negative (Table 2). Overall, in 40 of 306 nodal basins (13.1%), the hottest node was negative when a less radioactive node was positive. In 20 of these 40 (50%) basins, the positive, less radioactive sentinel node measured no more than 50% of the radioactive count of the hottest sentinel node. In two of 40 cases, the positive, less radioactive node measured < 10% of the hottest sentinel node; both of these cases were in the cervical nodal basin. In 35 of 40 basins in which the positive sentinel node was not the hottest node, the positive node was the first or second sentinel node identified in that basin.


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  		TABLE 2. Patients who would have had a false negative result if only the most radioactive ("hottest") node was removed
 
Overall, 69% of all sentinel nodes contained evidence of blue dye staining. However, 86.3% of the positive sentinel nodes contained blue staining, whereas only 66.4% of the histologically negative sentinel nodes contained blue staining. For cases in which the positive sentinel node was not the hottest node, blue dye staining was apparent in 31 of 37 cases (84%) in which blue dye was used.

Table 3 demonstrates the distribution of sentinel nodes within nodal basins. The cervical nodal basin was associated with an increased likelihood of finding the only positive sentinel node that was not the hottest node, or that was less than or equal to 50% of the ex vivo count of the hottest node.


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  		TABLE 3. Distribution of SLN within nodal basins
 
The impact of various definitions of a true sentinel node on the false-negative rate is demonstrated in Table 4. Although the actual false-negative rate can be established only by long-term follow-up to determine nodal recurrences in basins that were found to have negative sentinel nodes, removing all blue nodes and all nodes that contain 10% or more of the ex vivo count of the hottest node will minimize the false-negative rate. In the study so far, there have been seven false-negative results. In four of these cases, a single sentinel node was removed from the nodal basin. In the other three cases, the residual background activity after removal of the sentinel node(s) exceeded 10% of the ex vivo count of the hottest node. These factors suggest that further dissection and examination of those nodal basins may have demonstrated additional sentinel nodes that were microscopically positive at the time of SLN biopsy.


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  		TABLE 4. Impact of sentinel node definition on false-negative results
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Sentinel lymph node biopsy is a highly accurate method of staging regional lymph nodes for melanoma. By performing focused and detailed pathologic evaluation of the node or nodes most likely to contain metastatic disease, very early metastatic nodal disease is often detected. In the present study, 24.3% of patients with melanomas 1.0 mm or more in thickness were found to have histologic evidence of nodal metastasis. This is slightly higher than the rate in many other published series1–9 and indicates that the pathologic methods used are effective at detecting micrometastatic disease.

It is generally accepted that a blue lymphatic channel leading to a blue node is the gold standard for identification of the sentinel node. However, there may be two or more lymphatic channels leading to separate sentinel nodes. By using radioactive colloid injection with intraoperative gamma probe detection, it usually is possible to localize the sentinel nodes without relying completely on visualization of blue dye. As a practical matter, it may be possible to identify the first sentinel node with blue dye alone, but after that first node is dissected, it may be difficult to find additional nodes. It is very common, in fact, to localize the sentinel node with the gamma probe, only to find blue dye staining within the node in retrospect only after the node has been removed. Therefore, the gamma probe actually helps to identify blue nodes.

In most cases, the blue dye staining and radioactive colloid uptake correlate quite well in identifying the sentinel node(s). In other cases, for reasons that are not always clear, blue dye staining may not be obvious or it may not be easy to trace to the nodes. In fact, in the present study the positive sentinel nodes were not blue in 13.6% of cases.

The hand-held gamma counter facilitates detection of sentinel nodes by allowing transcutaneous localization of the site of the sentinel node, and it is possible to use the gamma probe intraoperatively to pinpoint the direction and location of the sentinel node or nodes. The gamma probe also is very helpful in identifying a second or third sentinel node, which often is difficult to detect after the first lymph node is removed when using blue dye alone. Therefore, the hand-held gamma counter may identify additional radioactive nodes that are identified as having blue staining only in retrospect, after they have been removed. Thus, the combination of blue dye and radioactive colloid may allow more accurate sentinel node identification because a second and third true sentinel node can be identified that might be missed with blue dye staining alone.

On occasion, multiple radioactive lymph nodes are detected after the most radioactive sentinel node has been removed. In some cases, the preoperative lymphoscintigram identifies what appears to be an entire chain of nodes, raising concern that the gamma probe will identify an inordinate number of radioactive nodes. In such cases it may be difficult to determine at what point these less radioactive lymph nodes should be removed. In the present study, 13.1% of the positive nodal basins would have been staged incorrectly if only the most radioactive lymph node was removed. In some cases, these less radioactive nodes were not blue, or were only faintly blue-stained and might have been missed if not for gamma probe detection. The cervical nodal basin appears most prone to have mildly radioactive nodes that are positive for tumor, which may be a reflection of the rich lymphatic drainage of the head and neck, and the occasional problems in head and neck melonomas with high background counts from the primary tumor site in close proximity to the nodal basin ("shine-through").

The results of this study indicate that all blue lymph nodes, as well as any lymph nodes remaining in the basin that contains 10% or more of the ex vivo count of the hottest sentinel node should be removed. Following this guideline will provide optimal detection of micrometastatic disease. Interestingly, a recent analysis of a large multi-institutional study found that this "10% rule" applies equally well to SLN biopsy for breast cancer.13 Even with this approach, the mean number of sentinel nodes removed was two per patient, and it is not common for more than three lymph nodes to fit these criteria, even when multiple nodes are seen on the lymphoscintigram.

These data provide practical guidelines for performance of SLN biopsy with optimal sensitivity. The Sunbelt Melanoma Trial will further investigate the role of adjuvant interferon alfa-2b for the treatment of patients with very early nodal metastases and determine the validity of reverse transcriptase polymerase chain reaction (RT-PCR) analysis as a molecular staging test for sentinel nodes and peripheral blood cells to determine patients at risk for recurrence or death.


   Acknowledgments
 
This study was supported by grants from Schering Oncology-Biotech, and the Center for Advanced Surgical Technologies (CAST) of Norton Hospital, Louisville, Kentucky. The authors wish to thank Carla Shelton, Kristi Recktenwald, Sherri Matthews, and Diana Simpson for their dedication and hard work on the Sunbelt Melanoma Trial.


   Footnotes
 
Preliminary findings presented at the annual meeting of the Society of Surgical Oncology, Orlando, Florida, March 4–7, 1999.

Received for publication April 3, 2000. Accepted for publication September 13, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Morton DL, Wen DR, Wong JH, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 1992; 127: 392–9.[Abstract]
  2. Albertini JJ, Cruse CW, Rapaport D, et al. Intraoperative radio-lympho-scintigraphy improves sentinel lymph node identification for patients with melanoma. Ann Surg 1996; 223: 217–24.[CrossRef][Medline]
  3. Gershenwald JE, Tseng CH, Thompson W, et al. Improved sentinel lymph node localization in patients with primary melanoma with the use of radiolabeled colloid. Surgery 1998; 124: 203–10.[Medline]
  4. Morton DL, Thompson JF, Essner R, et al. Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: a multicenter trial. Multicenter Selective Lymphadenectomy Trial Group Ann Surg 1999; 230: 453–63.
  5. Wells KE, Stadelmann WK, Rapaport DP, Hamlin R, Cruse CW, Reintgen D. Parotid selective lymphadenectomy in malignant melanoma. Ann Plast Surg 1999; 431: 1–6.
  6. Lenisa L, Santinami M, Belli F, et al. Sentinel node biopsy and selective lymph node dissection in cutaneous melanoma patients. J Exp Clin Cancer Res 1999; 18: 69–74.[Medline]
  7. Glass LF, Messina JL, Cruse W, et al. The use of intraoperative radiolymphoscintigraphy for sentinel node biopsy in patients with malignant melanoma. Dermatol Surg 1996; 22: 715–20.[CrossRef][Medline]
  8. Wells KE, Rapaport DP, Cruse CW, et al. Sentinel lymph node biopsy in melanoma of the head and neck. Plast Reconstr Surg 1997; 100: 591–4.[Medline]
  9. Bartolomei M, Testori A, Chinol M, et al. Sentinel node localization in cutaneous melanoma: lymphoscintigraphy with colloids and antibody fragments versus blue dye mapping. Eur J Nucl Med 1998; 25: 1489–94.[CrossRef][Medline]
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