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Right arrow Sentinel lymph node
Annals of Surgical Oncology 10:27-31 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Prediction of Nonsentinel Lymph Node Status in Melanoma

Mark E. Reeves, MD, PhD, Ruby Delgado, MD, Klaus J. Busam, MD, Mary S. Brady, MD and Daniel G. Coit, MD

From the Department of Surgery (MER), Loma Linda University and VA Medical Centers, Loma Linda, California; and the Departments of Surgery (MSB, DGC) and Pathology (RD, KJB), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Daniel G. Coit, MD, Gastric and Mixed Tumor Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 212-717-3400; E-mail: coitd{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Most melanoma patients with a positive sentinel lymph node dissection (SLND) undergo a completion lymph node dissection (CLND) that does not yield additional positive nonsentinel lymph nodes (NSLN). This study was designed to determine if NSLN status can be predicted using patient, primary tumor, and sentinel lymph node (SLN) characteristics.

Methods: The study population includes melanoma patients who had a positive SLND and subsequently underwent CLND retrieved from our prospective institutional melanoma database. The primary tumor and SLN pathologies were prospectively determined. An Size/Ulceration (SU) score was derived by assigning 1 point for primary tumor ulceration and 1 point for SLN tumor size >2 mm.

Results: Ninety-eight patients had a positive SLND and underwent CLND. Sixteen of these patients had a positive NSLN. On univariate analysis, primary tumor characteristics (thickness, ulceration, no regression), SLN metastasis characteristics (size >2 mm, location nonsubcapsular), and SU score were all significantly associated with positive NSLN status. However, on multivariate analysis, only the SU score was a significant independent predictor of NSLN status. No patient with an SU score of 0 had a positive NSLN.

Conclusions: The SU score is predictive of NSLN status in patients with a positive SLND. Patients with an SU score of 0 are very unlikely to have positive NSLNs at CLND.

Key Words: Melanoma • Sentinel lymph node dissection • Prediction • Nonsentinel lymph node


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sentinel lymph node dissection (SLND) provides a low-morbidity approach to accurate nodal staging for patients with melanoma.1–9 It provides important prognostic information, it can identify patients that might benefit from early nodal dissection, and it can define prognostically more homogeneous patient populations for entry into clinical trials.10 Because of this, SLND, followed by completion lymph node dissection (CLND) when sentinel lymph nodes (SLNs) are positive, has become a standard for management of intermediate and high-risk melanoma with clinically negative lymph nodes.6,11

Before the advent of SLND, elective lymph node dissection (ELND) was a favored management approach for patients with intermediate thickness melanoma and clinically negative lymph nodes. Although four prospective randomized trials have failed to demonstrate a survival advantage with routine ELND, at least one trial has suggested that there may be subsets of patients who might benefit from early aggressive regional lymph node intervention.12 One might postulate that a subset most likely to benefit might be those patients with clinically occult micrometastases in the regional nodes, as suggested by another of the prospective trials.13 However, SLND (with CLND only for those with a positive SLN) spares approximately 80% of these patients from the morbidity of an ELND because only 20% of SLNDs are positive in this patient population.3–8,14–16 The Multicenter Selective Lymphadenectomy Trial is studying the effect of this approach on survival.17 This trial randomizes patients with melanomas at least 1 mm thick or Clark level IV and clinically negative lymph nodes to SLND (and CLND if SLND is positive) or to observation after wide local excision. This should answer the question of whether SLND, followed by selective CLND for positive SLNs, has an impact on survival.

However, several prospective data series have also shown that only 15% to 20% of patients with a positive SLN will have a positive nonsentinel lymph node (NSLN) at CLND.4–6,8,15,16,18–20 Thus, only approximately 4% of patients with intermediate or high-risk melanoma that undergo a SLND will have tumor in a NSLN. Prior studies have used tumor thickness and SLN tumor volume to try to predict NSLN status.16,19,20 If NSLN status could be predicted, some patients with a positive SLND might not need a CLND. This study was designed to determine if NSLN status can be predicted based on patient, primary tumor, and SLN characteristics. In particular, we were looking for a factor or combination of factors that would identify a cohort of SLN-positive patients at no or very low risk of NSLN positivity.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
At Memorial Sloan-Kettering Cancer Center, patients with melanomas at least 1 mm thick or Clark level IV and clinically negative lymph nodes are candidates for SLND.21 A standard SLND procedure was used as previously described.22 Patients undergoing SLND were entered and followed in a prospective institutional melanoma database. This database was queried for patients that had a positive SLND and subsequently underwent CLND. Patient characteristics were retrieved from the database.

The primary tumor (n = 90) and SLN (n = 98) pathologies were prospectively determined by two dermatopathologists (K.J.B. and R.D.). The primary tumor pathology slides for eight patients who had the original excisional biopsy at an outside facility were not available for prospective review. SLNs were bivalved and stained with hematoxylin and eosin (H&E). If no tumor was found, they were immunohistochemically stained for S-100 and HMB-45. If tumor was still not found, the SLN was step-sectioned and stained with H&E (three sections) and S-100 and HMB-45 (two sections). SLN tumor size and location were determined. NSLN pathology in the CLND specimen was determined by H&E staining of bivalved lymph nodes.

Univariate and multivariate analyses using logistic regression were performed to determine which of the patient, tumor, and SLN characteristics might be predictive of NSLN positivity. Characteristics that achieved an odds ratio significantly different from one at a 95% confidence level on univariate analysis were entered into multivariate analysis. {chi}2 statistics were calculated for the analysis of the relationship between Size/Ulceration (SU) score and NSLN positivity. Confidence intervals at a 95% level were calculated for the number of NSLNs within each SU score category by the method of Clopper and Pearson.23


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Between 1991 and 2001, 659 patients underwent a SLND for melanoma at Memorial Sloan-Kettering Cancer Center. Of these, 98 (15%) had a positive SLN and underwent CLND. Sixteen of these patients (16%) had a positive NSLN at CLND.

Patient, Tumor, and SLN Characteristics
As expected for patients with positive SLNs, this population has high-risk characteristics (Table 1). Of note, half of the tumors were on the trunk, almost half were ulcerated, and the median thickness was 2.8 mm. On average, more than two lymph nodes were removed at each SLND, and more than 20 lymph nodes were removed at the CLND. Almost half of the positive SLNs contained less than 2 mm of tumor, but the tumor was detectable by H&E staining in three quarters of SLNs. On a lymph node basis, 50% of lymph nodes harvested at the time of SLND contained tumor, whereas only 2% of NSLNs harvested at CLND were positive.


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  		TABLE 1. Patient, tumor, and sentinel lymph node characteristics of 98 patients with a positive SLND who underwent CLND
 
Characteristics Predictive of NSLN Positivity
To determine which characteristics might be predictive of NSLN status, univariate and multivariate analyses of their association with NSLN positivity were performed (Table 2). On univariate analysis, three primary tumor characteristics (thickness, ulceration, and no regression) and two SLN metastasis characteristics (size >2 mm and nonsubcapsular location) were significantly associated with positive NSLN status. However, on multivariate analysis, none of these was a significant independent predictor of NSLN status.


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  		TABLE 2. Univariate and multivariate analyses of NSLN positivity without SU score
 
As no single patient, tumor, or SLN characteristic was absolutely predictive of NSLN status, we searched for a combination of characteristics that could identify patients at zero or low risk of having positive NSLNs. We derived a Size/Ulceration (SU) score by assigning 1 point for an ulcerated primary tumor, and 1 point for a SLN containing more than 2 mm of tumor. Thus, the SU score can range from 0 to 2. Univariate and multivariate analyses were again performed (Table 3). Because the SU score is directly calculated from ulceration and SLN tumor size, these two characteristics were not entered into the multivariate analysis for the SU score. On univariate analysis, thickness, no regression, nonsubcapsular location, and SU score were all significantly associated with NSLN positivity. However, only the SU score remained as a significant predictor of NSLN status on multivariate analysis.


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  		TABLE 3. Univariate and multivariate analyses of NSLN positivity with SU score
 
Relationship Between SU Score and NSLN Positivity
The relationship between SU score and NSLN positivity was analyzed more closely by determining the number of patients with various SU scores that had positive NSLNs at CLND (Table 4). No patient with an SU score of 0 had a positive NSLN at CLND. In addition, patients with an SU score of 2 were twice as likely to have positive NSLNs than patients with an SU score of 1.


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  		TABLE 4. Relationship between SU score and NSLN positivity
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The intergroup trial showed that ELND does not improve survival for patients overall. However, it identified patients with a lower risk of having systemic disease even with nodal metastases (nonulcerated, thin, extremity tumors; young patients) who might benefit from ELND.12 The World Health Organization trial of ELND in truncal melanoma was also negative overall. However, for patients with positive lymph nodes, survival was better for those who underwent ELND as opposed to therapeutic lymph node dissection.13 Thus, there may be subgroups of patients that might benefit from early lymph node dissection.

SLND may be able to define one such subgroup by accurately identifying those patients with clinically occult nodal metastases. If a selective lymphadenectomy algorithm is used in which only those patients with a positive SLND undergo CLND, approximately 80% of patients with intermediate and high-risk melanoma will be spared a lymph node dissection.3–8,14–16 Although we still do not know if this approach improves survival compared with lymph node dissection only when lymph nodes become clinically positive, the Multicenter Selective Lymphadenectomy Trial data should help to answer this question.17

One subset of patients that might be least likely to benefit from CLND are those with a positive SLND who do not have more positive NSLNs at CLND. In previous prospective data series, approximately 80% of patients with a positive SLND fall into this category (Table 5). Thus, even if early lymph node dissection is ultimately shown to improve survival, only 4% (20% of 20%) of patients that undergo a SLND are likely to benefit from a subsequent CLND. The remainder may be adequately staged and treated with a SLND alone. Therefore, it is important to identify these patients that are unlikely to have positive NSLNs and are thus unlikely to benefit from CLND. This study identifies these patients as those with an SU score of 0.


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  		TABLE 5. Selected series reporting CLND status after positive SLND
 
Other large prospective series of SLND for intermediate and high-risk melanoma report that approximately 20% of SLND are positive and approximately 20% of CLNDs have positive NSLNs.3–8,14–16,18–20 Our findings are similar: 15% of SLNDs were positive and 16% of CLNDs had positive NSLNs. Clearly, these results will vary depending on the types of patients being studied and the completeness of sentinel lymphadenectomy.5 However, these numbers are fairly consistent across multiple series because most centers use similar criteria for patient selection and techniques for SLND.

Others have also attempted to predict which patients would have positive NSLNs at CLND.16,19,20 Haddad suggested that primary tumor thickness may be important for predicting NSLN status.19 However, this has not been confirmed in other studies.16,24 In our study, patients with tumors as thin as 2.0 mm had positive NSLNs. Starz et al. have used a complicated scoring system based on the number of tumor-involved step sections and centripetal depth of tumor in the SLN to predict NSLN positivity.20 This system is complex and not widely reproducible in nondedicated pathology departments. The SU score that we have developed has several important attributes. First, it is easy to use and is based on primary tumor and SLN characteristics that are already measured by most melanoma pathologists. Second, it independently predicts NSLN status. Third, it varies proportionally with the risk of NSLN positivity.

Clearly, the results of this study need to be validated in other large prospective data series. Additionally, it is important to note that this study shows that the SU score can identify patients that are at low risk for having tumor in NSLNs detectable by H&E staining. It is certainly possible that H&E-negative NSLNs might actually contain residual tumor not detectable by H&E.25 However, the SU score is able to stratify patients according to risk of NSLN positivity using the methods that are currently standard for tumor detection in NSLNs.

In summary, although several tumor and SLN characteristics are associated with NSLN status on univariate analysis, in this study only the SU score is an independent predictor of NSLN positivity in patients with a positive SLND. Patients with an SU score of 0 are very unlikely to have positive NSLNs at CLND, and thus are unlikely to benefit from CLND.


   Footnotes
 
A Size/Ulceration (SU) score, based on primary tumor ulceration and sentinel lymph node tumor size, is predictive of nonsentinel lymph node status in patients with a positive sentinel lymph node dissection. Patients with an SU score of 0 are very unlikely to have positive nonsentinel lymph nodes at completion lymph node dissection.

Received for publication March 15, 2002. Accepted for publication September 12, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  12. Balch CM, Soong S, Ross MI, et al. Long-term results of a multi-institutional randomized trial comparing prognostic factors and surgical results for intermediate thickness melanomas (1.0 to 4.0 mm). Intergroup Melanoma Surgical Trial. Ann Surg Oncol 2000; 7: 87–97.[Abstract]
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