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Annals of Surgical Oncology 10:569-574 (2003)
© 2003 Society of Surgical Oncology

NEW APPROACHES TO THE TREATMENT OF HEPATIC MALIGNANCIES

Revised American Joint Committee on Cancer Staging Criteria Accurately Predict Sentinel Lymph Node Positivity in Clinically Node-Negative Melanoma Patients

Dennis L. Rousseau, Jr, MD, PhD, Merrick I. Ross, MD, Marcella M. Johnson, MS, Victor G. Prieto, MD, PhD, Jeffrey E. Lee, MD, Paul F. Mansfield, MD and Jeffrey E. Gershenwald, MD

From the Departments of Surgical Oncology (DLR, MIR, JEL, PFM, JEG), Biostatistics (MMJ), and Pathology (VGP), The University of Texas M. D. Anderson Cancer Center, Houston, Texas.

Correspondence: Address correspondence and reprint requests to: Jeffrey E. Gershenwald, MD, Department of Surgical Oncology, Box 444, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030; Fax: 713-745-4926; E-mail: jgershen{at}mdanderson.org

ABSTRACT

Background: The American Joint Committee on Cancer (AJCC) has recently modified staging criteria for primary melanoma patients and recommends sentinel lymph node (SLN) biopsy in many because microscopic nodal metastasis represents the most important factor predicting survival. The purpose of this study was to correlate the incidence of SLN metastasis with revised AJCC staging.

Methods: The records of 1375 melanoma patients undergoing SLN biopsy were reviewed. Univariate and multivariate analyses were performed to identify predictors of a positive SLN. Patients were stratified by using revised AJCC criteria to determine whether such groups also predicted positive SLNs.

Results: A positive SLN was found in 16.9% of patients. By multivariate analysis, tumor thickness (relative risk [RR], 3.4) and ulceration (RR, 2.2) were dominant independent predictors of SLN metastases; age <=50 years (RR, 1.8) and axial tumor location (RR, 1.5) were also significant. When patients were stratified by AJCC staging criteria, a significant increase in SLN metastases between successive stages was demonstrated.

Conclusions: Stratification of patients by using AJCC classification reveals an increasing risk of SLN metastases with successive stage groups. Given the significant association of SLN status and survival, the ability of the revised AJCC staging system to predict survival is likely due to its ability to predict the risk of occult nodal disease.

Key Words: Sentinel lymph node • Staging • Melanoma • Metastasis

An estimated 54,200 new cases of melanoma will be diagnosed in the United States in the year 2003, resulting in 7600 deaths.1 The vast majority of these patients will present with clinically localized disease—i.e., without evidence of clinical lymph node involvement (stages I and II). As our understanding of the natural history of this disease and its risk factors has improved, physicians have learned to identify those patients with an increased risk of metastatic disease and poor survival. One of the most important factors for survival in the clinically node-negative patient is the histological status of the regional lymph node basin.2,3

Recently, several factors important for early stage melanoma survival have been discovered3 and incorporated into the 2002 American Joint Committee on Cancer (AJCC) T-category classification for stage I/II melanoma patients (Table 1).4,5 Although tumor thickness and ulceration have been shown to be the predominant independent predictors of survival, pathologic nodal staging was not routinely performed in the vast majority of these patients. The technique of lymphatic mapping and sentinel lymph node (SLN) biopsy has become the standard method for determining the pathologic status of the regional lymph node basin in many patients with primary cutaneous melanoma.2,6–11 Knowledge of the status of the SLN is the most important factor with respect to survival in clinically node-negative melanoma patients.2,3,10,11 In addition, independent predictors of SLN metastases have been identified by contemporary multivariate analyses and include tumor thickness,8,12–14 ulceration,8,12–14 high mitotic index, 12 multiple nodal basin drainage, 13 and patient age and Clark level.14 Knowledge of the factors associated with a positive SLN would be useful for counseling patients regarding treatment options and possible outcomes.


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  		TABLE 1. 2002 AJCC melanoma T classification4
 
In this study, we sought to better understand which of the known clinicopathologic prognostic factors—tumor thickness, ulceration, Clark level, age, sex, and site of the primary lesion—could be used to predict the risk of SLN metastasis in a large cohort of patients who underwent successful SLN biopsy. We then classified patients by the revised AJCC staging system to determine whether the new stage groupings had predictive value regarding the presence of a positive SLN.

PATIENTS AND METHODS

Patients
By using a prospective surgical melanoma database, 1375 patients with primary cutaneous melanoma who underwent successful intraoperative lymphatic mapping and SLN biopsy at the University of Texas M. D. Anderson Cancer Center from 1991 to May 2001 were identified. In general, patients were offered this procedure if (1) their primary tumor was at least 1.0 mm thick; (2) tumors were Clark level IV or had evidence of ulceration, regression, or vertical growth phase, if <1.0 mm; (3) there was no clinical evidence of regional nodal spread; and 4) there was no evidence of distant metastatic disease as assessed by clinical examination, chest radiography, and serum lactate dehydrogenase level. All 1375 patients had sufficient information for classification with the revised AJCC staging criteria. Of these 1375 patients, 1351 patients (>98%) had complete information for the prognostic factor analysis.

SLN Mapping Technique
Intraoperative lymphatic mapping and SLN biopsy were performed as described previously.2,8,15 From 1991 to 1994, intraoperative lymphatic mapping and SLN biopsy was performed by using isosulfan blue dye only. For the procedure, 1 to 3 mL of dye was injected intradermally around the tumor or biopsy site just before mapping. In the overwhelming majority of cases (November 1994 to present), this procedure also included intradermal injection of .5 to 1 mCi of 99mTc-labeled sulfur colloid 1 to 4 hours before mapping. Intraoperative localization of the SLN was aided by the use of a handheld gamma counter (Neoprobe 1500 or Neoprobe Neo 2000; Neoprobe, Dublin, OH). Most patients with primary lesions of the head and neck, trunk, and distal extremities underwent preoperative lymphoscintigraphy with intradermal injection of 99mTc-labeled sulfur colloid to identify lymph node basins at risk. An SLN was defined as a lymph node that was stained with blue dye, concentrated radiolabeled colloid, or both. Patients underwent wide local excision of the primary lesion with margins appropriate for tumor thickness.16,17 All patients with a positive SLN were offered completion therapeutic lymph node dissection. Initially, SLNs were bisected and analyzed by conventional hematoxylin and eosin staining; in cases of equivocal findings, immunohistochemistry with antisera to S-100 protein and melanoma antigen HMB-45 was performed to confirm the diagnosis. Currently, our standard histological assessment includes both gross specimen serial sectioning (since 1996) and immunohistochemical staining for HMB-45, MART-1, or both (since 1999) if the initial analysis fails to identify the presence of metastases.18

Statistical Methods
Clinicopathologic factors, including age, sex, tumor thickness, tumor location, presence of ulceration, and Clark level, were assessed as potential predictors of SLN positivity by using multivariate logistical regression models. A dichotomous age variable was created by using the median age of all patients as the cutpoint. Because the data for tumor depth were not normally distributed, various transformations of tumor depth were evaluated. The square-root transformation was selected for normalization properties and for ease of interpretation. The association of categorical variables was evaluated by using a {chi}2 or Fisher’s exact test, as appropriate. Furthermore, logistical regression models were used to determine the relative risks of AJCC staging on SLN positivity. All reported P values are two sided at a significance level of 5%. Analyses were performed with SAS for Windows (release 8.2; SAS Institute Inc., Cary, NC).

RESULTS

Clinicopathologic Factors
The clinical and pathologic characteristics for all 1375 patients are listed in Table 2. The median tumor thickness was 1.5 mm (mean, 2.2 mm). The median age was 51 years, and 58% of patients were male. Primary tumors were in an axial location in 52% of patients; ulceration of the primary tumor was present in 21% of patients. The overall incidence of SLN metastases was 16.9%.


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  		TABLE 2. Clinical and pathologic characteristics (n = 1375)
 
Univariate and Multiple Logistical Regression Analyses
The incidence of a positive SLN according to clinicopathologic factors is listed in Table 3. Tumor thickness, Clark level, and ulceration were the most significant predictors of SLN metastases by univariate analysis. Age <=50 years and axial location of the primary tumor were also significant univariate predictors of SLN metastases.


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  		TABLE 3. Incidence of a positive SLN according to clinicopathologic prognostic factors (n = 1375)
 
In a multivariate logistical regression model that included all covariates under consideration, tumor thickness (P < .0001; odds ratio [OR], 3.42) and presence of ulceration (P < .0001; OR, 2.21) were the dominant predictors of SLN metastasis (Table 4). Age <=50 years (P = .0003; OR, 1.81) and axial location of the primary tumor (P = .024; OR, 1.45) were also significant predictors of a positive SLN. Clark level and sex did not independently predict SLN metastasis in this analysis.


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  		TABLE 4. Multivariate analysis of prognostic factors for predicting SLN metastases (n = 1351)
 
Effect of Tumor Thickness and Ulceration
Because tumor thickness and ulceration were the dominant independent predictors of a positive SLN, the same two factors that were shown to be the most powerful predictors of survival in the AJCC multivariate analysis,3 we examined the interaction of these factors on SLN status within revised AJCC tumor thickness groupings (Table 5). When grouped by tumor thickness, there was an increased incidence of a positive SLN, ranging from 4% to 44%, among patients with melanomas by increasing tumor thickness from <=1.00 to >4.00 mm, respectively. In a similar fashion, when patients were stratified solely by the presence of primary tumor ulceration, patients with ulcerated primary tumors had a higher incidence of SLN metastases compared with those with nonulcerated lesions (35% vs. 12%; P < .0001). Moreover, when stratified by both ulceration and tumor thickness grouping, patients with ulcerated primary lesions had a greater incidence of a positive SLN compared with those without evidence of ulceration within any of the tumor thickness strata. The difference was most notable for the thin (<=1.00 mm) and thick (>4.00 mm) tumors, where patients with ulcerated versus nonulcerated lesions had an incidence of positive SLNs of 16% vs. 3% (P = .026) and 53% vs. 33% (P = .021), respectively. The presence of primary tumor ulceration increases the SLN positivity risk to that of patients without ulceration in the next higher tumor thickness strata (Table 5).


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  		TABLE 5. The effect of ulceration on SLN metastases for a given tumor thickness (n = 1375)
 
Incidence of SLN Positivity According to AJCC Categories
The revised AJCC staging criteria use tumor thickness and presence or absence of ulceration to define T categories (Table 1). In the thin melanoma, or T1 category, Clark level data are also used to classify patients.4,5 To examine the incidence of SLN metastases by AJCC classification, the 1375 patients were staged by using the new AJCC criteria. The incidence of positive SLNs by the revised AJCC T categories for this patient population is shown in Fig. 1. The actual incidence of SLN positivity for each T category is shown in the inset. Comparison of the incidence of SLN metastases with AJCC T category demonstrates that there is no significant difference between T2b and T3a (stage IIA) or between T3b and T4a (stage IIB).



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  		FIG. 1. Incidence of a positive sentinel lymph node (SLN) by American Joint Committee on Cancer T category (n = 1375). The inset shows the percentage of patients with a positive SLN within each category.

 
The incidence of SLN metastases by AJCC stage is represented in Fig. 2. Stage IA patients had a 2% incidence of SLN metastases. The incidence rates for stages IB, IIA, IIB, and IIC were 9%, 24%, 34%, and 53%, respectively, and represent statistically different risks at each substage (P < .0001). The relative risk of finding a positive SLN in these clinically node-negative patients based on AJCC staging is listed in Table 6. For this analysis, stage IA was the reference stage, with an OR of 1, and all other stages were compared with the reference stage. There is a marked stepwise increase in risk with increasing stage, with a maximum of a 40-fold increase in risk of a positive SLN when comparing stage IIC disease with stage IA disease.



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  		FIG. 2. Incidence of a positive sentinel lymph node (SLN) by American Joint Committee on Cancer stage (n = 1375). The inset contains the percentage of patients with a positive SLN within each stage. The difference between stages is statistically significant with the following P values: IA versus IB, P = .0003; IB versus IIA, P < .0001; IIA versus IIB, P = .041; and IIB versus IIC, P = .003.

 

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  		TABLE 6. Relative risk of finding a positive SLN by AJCC stagea
 
DISCUSSION

In the formal analysis conducted by the Melanoma Task Force of the AJCC, which validated the recently published revisions to the melanoma staging system, tumor thickness, ulceration, age, site of primary tumor, Clark level, and sex were all significant prognostic factors for survival, in descending order of importance.3 We examined these prognostic factors for their ability to predict the presence of SLN metastases in clinically node-negative patients. In our analysis, tumor thickness, ulceration, age <=50 years, and axial location of the primary lesion were independent predictors of an increased risk of SLN metastases.

Both tumor thickness and ulceration are well recognized as important predictors of survival.2,3,14 They have also been shown to be predictive of SLN metastases.8,12–14 Our study confirms these observations that tumor thickness (OR, 3.42; P < .0001) and ulceration (OR, 2.21; P < .0001) are the dominant factors in predicting the presence of occult nodal disease.

In this study, age <=50 years (the median of this data set was 51 years) was an independent predictor of SLN metastases (OR, 1.81; P < .0003). This association of younger age and the presence of a positive SLN does not have an obvious explanation. This result reproduces a similar finding by McMasters et al.14 that younger age was an adverse prognostic factor for the presence of SLN metastases. Reconciling this observation with the observation that younger age portends a better survival prognosis3,19 will require further analysis of the age subsets to determine whether there are significant age-related differences in the natural history of this disease.

Before this study, axial location of the primary lesion (i.e., trunk or head and neck) was not identified as an independent predictor of SLN metastases.8,14 In this multivariate analysis, axial location was a significant predictor of a positive SLN (OR, 1.45; P = .026). In truncal melanoma, the presence of multiple nodal basin drainage is a significant risk factor for SLN metastases.13 In our study population, the incidence of multiple nodal basin drainage was higher in the axial group as compared with the extremity group (32% vs. 4%), which could explain why axial location of the tumor is a predictor of the presence of SLN disease. This finding emphasizes the importance of the use of preoperative lymphoscintigraphy in patients with axial lesions,20–23 because this allows more accurate determination of lesions with multiple nodal basin drainage and more complete staging of these patients.

The finding that Clark level was not an independent predictor of SLN metastases is consistent with prior reports.8,12 In contrast, McMasters et al.14 reported that Clark level was a significant predictor in their multivariate analysis. The reason for this discrepancy is not obvious but may reflect differences in the inclusion criteria for each study, especially the inclusion of thin-melanoma (<1.00 mm) patients in this study. Future large database analyses of thin-melanoma patients should help clarify the effect of Clark level as a prognostic factor for the presence of a positive SLN.

Although the validation study of the revised AJCC staging system3 demonstrated that tumor thickness and ulceration were the dominant predictors of survival, most of these node-negative patients did not have pathologic regional nodal staging. In this study, because all patients underwent SLN biopsy, we were able to examine whether the revised staging system accurately predicts the presence of SLN metastases in the clinically node-negative patient population. It is interesting to note that when the positive SLN data are stratified by these revised AJCC survival-based groupings (Fig. 2 and Table 5), the increased risk of a positive SLN with increasing stage parallels the trend observed in the AJCC survival analysis (Table 1).

In conclusion, tumor thickness and ulceration were the dominant independent predictors of SLN metastases in patients with clinically negative regional lymph nodes. The revised AJCC staging system accurately stratified clinically node-negative patients by their risk of harboring sentinel nodal metastases. Indeed, given the important relationship of SLN status and survival (Fig. 2 and Table 1), the ability of the revised AJCC classification system to predict survival is likely due to its ability to accurately predict the risk of occult nodal disease. Knowledge of both prognostic factors for SLN metastases and the incidence of SLN metastases relative to AJCC stage will be a useful addition in clinical practice, especially in the counseling of treatment options for clinically node-negative patients.

Acknowledgments

The authors thank the Department of Scientific Publications for their assistance with this manuscript. Supported in part by an award from the University of Texas M. D. Anderson Physician-Scientist Program (JEG) and a National Institutes of Health T-32 grant CA09599 (DLR).

The acknowledgments are available online at www.annalssurgicaloncology.org.

Footnotes

Presented at the Society of Surgical Oncology Annual Meeting, Denver, Colorado, March 14–17, 2002.

In this study of 1375 clinically node-negative cutaneous melanoma patients, tumor thickness, ulceration, younger age, and axial location were independent predictors of sentinel lymph node metastases. Classifying patients by using the revised American Joint Committee on Cancer staging criteria accurately reflected an increasing risk of occult nodal disease.

Received for publication September 24, 2002. Accepted for publication January 13, 2003.

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