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Annals of Surgical Oncology 9:137-141 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Frequency of Nonsentinel Lymph Node Metastasis in Melanoma

Kelly M. McMasters, MD, PhD, Sandra L. Wong, MD, Michael J. Edwards, MD, Celia Chao, MD, Merrick I. Ross, MD, R. Dirk Noyes, MD, Vicki Viar, RN, MSN, Patricia B. Cerrito, PhD and Douglas S. Reintgen, MD for the Sunbelt Melanoma Trial Group

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

Correspondence: Address correspondence and reprint requests to: Kelly M. McMasters, MD, PhD, University of Louisville–Brown Cancer Center, 529 S. Jackson St., Louisville, KY 40202; Fax: 502-629-3393; E-mail: kelly.mcmasters{at}nortonhealthcare.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Completion lymph node dissection (CLND) may not be necessary for some patients because nodal metastasis is rarely detected beyond the sentinel lymph nodes (SLNs). This analysis was performed to determine, among patients with positive SLNs, the rate of nodal metastasis found in nonsentinel nodes (NSNs).

Methods: This analysis includes patients with positive sentinel nodes, detected by hematoxylin and eosin (H&E) staining or immunohistochemistry (IHC), who then underwent CLND.

Results: This analysis included 274 patients with at least one positive SLN who underwent CLND of 282 involved regional nodal basins. Of the 282 SLN-positive nodal basins, 45 (16%) were found to have positive NSNs in the CLND specimen. Breslow thickness, Clark level, presence of ulceration, histological subtype, presence of vertical growth phase, evidence of regression, presence of lymphovascular invasion, number of positive SLNs, age, sex, and presence of multiple draining nodal basins were not predictive of positive nodes in the CLND specimen. Patients with SLN metastases detected only by IHC had an equal likelihood of having positive NSNs as those patients with positive SLNs on H&E examination.

Conclusions: No patient population could be identified with minimal risk of non-SLN metastasis. When a positive SLN is identified on either H&E staining or IHC, CLND should be performed routinely.

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


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
An estimated 51,400 patients in the United States will be newly diagnosed with malignant melanoma, and 7,800 will die of this disease1 in 2001. It has long been recognized that involvement of the regional lymph nodes is the most important prognostic factor for patients with melanoma. Indeed, the presence of lymph node metastases decreases the 5-year survival of patients by approximately 40%, independent of other prognostic factors of the primary tumor.2

Sentinel lymph node (SLN) biopsy has become widely accepted as a method of staging the regional lymph nodes in patients with melanoma. SLN biopsy can be performed on an outpatient basis at the same time as wide local excision of the primary melanoma. It is less morbid than an elective lymph node dissection (ELND) and is cost-effective.3,4 The advantage of SLN biopsy in melanoma is that it spares 75%–80% of patients the need for complete regional lymphadenectomy while identifying those patients at highest risk. The presence of a positive sentinel node has been shown to be the single most important prognostic factor for recurrence and survival.5 Those patients with positive SLN are appropriately selected for therapeutic completion lymph node dissection (CLND) and adjuvant therapy.

Previous studies have suggested that there may be some melanoma patients for whom CLND may not be necessary because nodal metastasis was never detected beyond the sentinel nodes.6–8 This analysis was performed to determine, among patients with positive SLNs, the rate of nodal metastasis in the CLND specimen. Further, we sought to identify factors predictive of a minimal risk of positive CLND.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The Sunbelt Melanoma Trial is a multicenter, prospective, randomized study involving 70 centers across the United States. Patients enrolled from June 1997 to February 2001 were included in this analysis. The study was approved by the institutional review boards of the participating institutions. Patients in this analysis were entered from 46 different institutions. Eligibility criteria included patient age 18 to 70 years, cutaneous melanomas >=1.0-mm Breslow thickness, and clinically negative regional lymph nodes.

After informed consent was obtained, patients underwent wide local excision of the primary melanoma and SLN biopsy with intradermal injection of isosulfan blue dye and 99mTc-labeled sulfur colloid around the site of the primary tumor. Lymphoscintigraphy was performed to identify all draining nodal basins and ectopic or in-transit sentinel nodes. A handheld gamma probe was used intraoperatively along with visualization of blue dye to guide SLN detection. The protocol specified that all blue nodes and all nodes >=10% of the most radioactive, or hottest, node should be removed and designated SLNs.9

All sentinel nodes underwent histological analysis with hematoxylin and eosin (H&E) staining at multiple levels, followed by immunohistochemistry (IHC) for S-100 protein. Sentinel nodes were divided into blocks on the basis of lymph node size; at least five sections per block were evaluated by H&E staining and two sections per block by IHC. Immunohistochemical staining for HMB-45 or MART-1 was performed selectively at a few institutions as well. The primary melanoma and SLN pathology from the first 10 cases from each institution, as well as all cases of a positive SLN, were reviewed by a central pathology review committee. The CLND specimens were not evaluated by the pathology review committee. As part of the Sunbelt Melanoma Trial, reverse transcriptase–polymerase chain reaction (RT-PCR) analysis of SLNs was performed to detect the presence of occult melanoma cells. However, RT-PCR–positive patients who had subsequent CLND were not included in this analysis.

Patients found to have an SLN with metastatic disease by H&E staining, IHC, or both underwent CLND of the involved nodal basin or basins. Nonsentinel nodes (NSNs) were evaluated by routine H&E staining (not by serial sectioning or IHC). Statistical comparison was performed with {chi}2 analysis. Significance was determined at P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
This analysis includes 274 patients with at least one positive SLN who underwent CLND of 282 involved regional nodal basins. Patient clinicopathologic characteristics are listed in Table 1. Of the 282 SLN-positive nodal basins, 45 (16%) were found to have positive nodes in their CLND specimen.


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  		TABLE 1. Clinicopathologic features of the patient population
 
Prognostic factors included in the statistical model were as follows: Breslow thickness, Clark level, presence of ulceration, histological subtype, presence of vertical growth phase, evidence of regression, presence of lymphovascular invasion, number of positive SLNs, age, and presence of multiple draining nodal basins. As shown in Table 2, none of these factors was predictive, by univariate analysis, of positive nodes on CLND when the SLN biopsy was positive. Multivariate analysis, therefore, was not performed. When the subgroup of patients with melanomas of <1.5-mm Breslow thickness was evaluated, 5 (8.9%) of 56 patients had positive NSNs.


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  		TABLE 2. Factors associated with nonsentinel lymph node positivity
 
Patients with SLNs positive for metastatic disease noted only on IHC staining had a similar incidence of disease in the CLND specimen as those patients with H&E-positive SLNs (Table 3). There were no significant differences in the rate of SLN positivity for centers that used HMB-45 or MART-1 immunostains.


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  		TABLE 3. CLND results in patients with IHC-only positive SLNs
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
SLN biopsy has been shown to be an accurate method of staging the regional nodal basins in patients with melanoma. Several studies have found that the sentinel node was the only site of metastatic disease in the regional lymph node basin in the majority of cases. However, residual disease in the NSN has been reported5–7,10–17 with an incidence of 7% to 33%. In particular, it has been suggested that patients with primary tumors <1.5 mm thick may be able to avoid CLND because NSN metastases are so rare in this population.6,7 Haddad et al.8 even suggested that CLND may be avoided in patients with positive SLNs and primary tumor thickness <2.8 mm.

This analysis represents the largest study to date to evaluate the factors associated with positive NSNs. Our study demonstrates an overall 16% incidence of residual disease in NSNs when positive SLNs are found. Furthermore, 9% of patients with tumors 1.0- to 1.5-mm Breslow thickness had positive NSNs. We also examined the following factors to determine whether there was an association with positive NSNs: Clark level, presence of ulceration, vertical growth phase, regression, lymphovascular invasion, histological subtype, number of positive SLNs, age, and number of draining nodal basins. No factor predictive of minimal risk of NSN metastases could be identified.

We have previously shown that increasing Breslow thickness, Clark level, ulceration, and patient age were independent factors predictive of positive SLN results.18 These variables were not associated with the presence of positive NSNs in the CLND specimen in this analysis. However, we cannot discount the possibility that factors such as tumor thickness, Clark level, and the number of positive SLNs might reach statistical significance as predictive factors, given a larger sample size. The important point, however, is that once a positive SLN was found, even the patients with the most favorable primary melanomas had a substantial risk of NSN metastasis in this large multicenter study.

Wagner et al.16 reported positive NSNs in 28.3% of patients after the finding of a positive SLN. Consistent with our results, no relationship between primary melanoma tumor characteristics and the presence of disease in NSN could be demonstrated in their study. On univariate analysis, positive nodes in the completion lymphadenectomy specimen were associated only with findings of multiple positive SLNs. The same group reported a similar correlation between positive NSNs and multiple positive SLNs in patients with primary melanomas of the head and neck.19

In this study, we also examined the relationship between the presence of metastases in multiple SLNs and positive NSNs. We found that when more than one SLN contained evidence of metastatic disease, the rate of NSN metastases was actually lower than if only one SLN was positive, although that result was not statistically significant.

It is likely that we underestimated the amount of residual disease in the CLND specimen because the NSNs were not subjected to the same rigorous histopathologic examination as the SLNs. Indeed, positive SLNs would have been missed in 51 (18.1%) of 282 positive nodal basins had IHC not been used. Furthermore, 13.7% of these IHC-only positive sentinel nodes had H&E-positive nodes in the CLND specimen. This is supporting evidence for the diagnostic value of IHC-detected SLN micrometastasis in melanoma. We have also found that RT-PCR analysis will detect the presence of occult melanoma cells in the NSNs of approximately 50% of patients who undergo CLND for a positive SLN.20 Many studies have retrospectively re-examined the sentinel nodes in patients who were thought to have a negative SLN on initial evaluation but later developed regional lymph node recurrences (false-negative SLN results). These studies have demonstrated occult SLN metastatic disease in 36% to 80% of patients.7,15,21–23

SLN biopsy is a minimally invasive procedure that accurately identifies those high-risk patients who may benefit from early CLND. It should be emphasized that patients with positive NSNs had obvious nodal metastatic disease detected on routine H&E evaluation, which usually involves bivalving each lymph node and examining one or two representative sections through the center of the node. Therefore, the NSN metastases detected in this study represent nodal disease that would probably result in the development of future palpable nodal metastasis if CLND was not performed.

We still do not know whether SLN biopsy, with subsequent CLND for patients with positive SLNs, improves survival. An ongoing study, the Multicenter Selective Lymphadenectomy Trial by Morton et al.,24 will address the effect of SLN biopsy on survival. While we await the results of this study, there are some data to suggest that early therapeutic lymphadenectomy for patients with microscopically positive lymph nodes may improve survival. The 10-year follow-up results for the Intergroup Melanoma Surgical Trial demonstrated a 4% overall survival advantage in favor of ELND, although this did not reach statistical significance.25,26 However, certain prospectively stratified subgroups of patients, specifically those with nonulcerated melanomas, extremity melanomas, and primary tumors from 1- to 2-mm Breslow thickness did demonstrate a significant overall survival benefit from ELND. Although retrospective subgroup analysis of clinical trials is always subject to criticism, it is important to point out that patients in this study were prospectively stratified by tumor thickness, anatomical site, and ulceration, and these analyses were planned during the design of the trial. Another crucial piece of evidence regarding the value of early lymph node dissection versus delayed dissection for nodal disease is derived from the World Health Organization Program 14 Trial of ELND for patients with truncal melanomas.27 Overall, there was no difference in survival for the two randomized arms (nodal observation vs. ELND). However, when the survival of the patients with positive lymph nodes, either detected histologically at ELND or by palpation in the observation arm, is considered, quite a different picture emerges. The overall survival of patients with nodal micrometastases removed at ELND was significantly greater than that of patients who underwent lymphadenectomy for palpable lymph nodes in the observation arm (48.2% vs. 26.6% 5-year survival; P = .04). Together, these two studies support the rationale for early therapeutic lymph node dissection in patients with clinically negative, but pathologically positive, lymph nodes.

The other goal of SLN biopsy is to identify patients with nodal metastasis who may benefit from adjuvant therapy. Adjuvant therapy with high-dose interferon alfa-2b has been shown to improve disease-free (3 of 3 studies) and overall (2 of 3 studies) survival for patients with high-risk melanoma.28–30 Furthermore, an interim analysis of the European Organization for Research and Treatment of Cancer study 18952 was recently presented, showing that intermediate doses of interferon alfa-2b significantly improved distant metastasis-free survival (A. Eggermont, personal communication, March 2001). Whether or not adjuvant interferon alfa-2b is effective in reducing the risk of nodal metastasis among patients with a positive SLN who do not undergo CLND is not known. This may be an appropriate subject for future clinical trials. Until such information is available, we recommend CLND for patients with a positive sentinel node because of the substantial risk of residual nodal disease.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
In this study, no patient population could be identified with minimal risk of NSN metastasis. When a positive SLN is identified, CLND should be performed routinely.


   Acknowledgments
 
Supported by a grant from Schering Oncology-Biotech and the Center for Advanced Surgical Technologies (CAST) of Norton Hospital, Louisville, KY. The authors wish to thank Carla Shelton, Sherri Matthews, and Diana Simpson for their continued dedication to the data management and coordination of this study.


   Footnotes
 
Presented at the 54th Annual Cancer Symposium of the Society of Surgical Oncology, Washington, DC, March 15–18, 2001.

Received for publication March 16, 2001. Accepted for publication September 20, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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