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10.1245/ASO.2006.02.021
Annals of Surgical Oncology 13:302-309 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Results of Sentinel Lymph Node Biopsy in Patients With Thin Melanoma

Sandra L. Wong, MD1, Mary S. Brady, MD1, Klaus J. Busam, MD2 and Daniel G. Coit, MD1

1 Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021
2 Department of Pathology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021

Correspondence: Address correspondence and reprint requests to: Daniel G. Coit, MD; E-mail: coitd{at}mskcc.org.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Sentinel lymph node (SLN) biopsy has been shown to be a highly accurate method of staging nodal basins in melanoma patients. Although this technique is widely accepted in patients with intermediate-thickness tumors, it is unclear what the indications are for thin (≤1 mm) melanoma.

Methods: From May 1991 to October 2004, 223 patients with thin melanoma underwent SLN biopsy at Memorial Sloan-Kettering Cancer Center. Most patients with thin melanoma were selected for the procedure because of high-risk clinicopathologic features.

Results: Nodal metastases were found in eight patients (3.6%) who underwent SLN biopsy. All positive SLNs were found in patients with ≥.75 mm-thick and Clark level IV melanoma (8 of 114; 7%). Age, sex, tumor location, thickness, Clark level, ulceration, regression, tumorin-infiltrating lymphocytes, mitotic rate, and number of mapped nodal basins were not predictive of positive SLNs ({chi}2; P = not significant). With a median follow-up of 25 months, there have been no recurrences or deaths in patients with melanoma <.75 mm. Six patients have had regional and/or systemic recurrences (2.7%), only one of whom had a positive SLN. Three patients have died of melanoma; all had negative SLNs.

Conclusions: Nodal metastasis in thin melanoma is uncommon, especially in patients with <.75 mm and Clark level II or III melanoma. In our experience, no single clinicopathologic factor was predictive of nodal metastases. The prognostic implications of positive SLNs in thin melanoma remain undefined.

Key Words: Thin melanoma • Sentinel node • Prognosis • Incidence • Predictors


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Sentinel lymph node (SLN) biopsy has been shown to be a highly accurate method of staging nodal basins at risk for regional metastasis in patients with primary cutaneous melanoma. Whereas this technique is widely accepted in patients with tumors >1 mm in thickness, the indications for SLN biopsy in patients with thin (≤1 mm) melanoma are less clearly defined.

Thin melanomas account for approximately 70% of all cutaneous melanomas and have historically been associated with an excellent prognosis. Long-term follow-up studies have shown that some thin melanomas are associated with aggressive tumor biology that leads to disease recurrence and death.1,2 The ability to determine which patients are at risk for recurrence or metastasis may help to identify ideal candidates for SLN biopsy. Patients with thin melanoma and associated high-risk factors such as ulceration, regression, or a Clark level of IV or higher have been increasingly selected for SLN biopsy. Extension of the procedure to this subset of patients has been performed in an attempt to improve staging and better predict prognosis.

Although SLN biopsy is a minimally invasive procedure, it should not be used indiscriminately. There is no consensus as to which prognostic factors are most predictive of regional metastases in thin melanoma. The purpose of this study was to examine a large single institution’s experience with SLN biopsy for thin melanoma to determine the incidence of SLN metastasis, to identify clinicopathologic predictors of positive SLN biopsy, and to evaluate the clinical significance of SLN status in terms of tumor recurrence and survival.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
A prospectively maintained database at Memorial Sloan-Kettering Cancer Center was queried for all patients with melanoma ≤1 mm who underwent SLN biopsy. SLN biopsy is not performed routinely for all patients with thin melanoma. Most patients in the study population were selected for the procedure because of high-risk clinicopathologic features of the primary tumor, usually a Clark level of IV or higher, ulceration, or both. We identified a consecutive series of patients with thin primary cutaneous melanoma who underwent successful SLN mapping and biopsy from May 1991 to October 2004. All primary tumor specimens from outside hospitals were routinely reviewed by pathologists at our institution before definitive treatment. Tumor thickness was based on final pathology results from the definitive excision of the primary melanoma. Patients with an unconfirmed histopathologic diagnosis of thin cutaneous melanoma, clinically suspicious lymphadenopathy, or failed lymphatic mapping were excluded from analysis.

SLN biopsy was performed by using intradermal 99mTc sulfur colloid and isosulfan blue dye injection. Preoperative lymphoscintigraphy was performed to map all draining nodal basins; a handheld gamma probe was used to identify radioactive counts during surgery. All blue nodes and all nodes with counts ≥10% of the ex vivo measurement of the hottest node were removed and designated as SLNs. Histopathologic analysis of serially sectioned specimens was performed by using hematoxylin and eosin staining and immunohistochemical analysis (S-100 and HMB-45) if the initial hematoxylin and eosin examination did not reveal metastatic disease. Patients with positive SLNs underwent completion lymphadenectomy of the involved nodal basin.

Clinicopathologic factors such as age, sex, site of the primary lesion, tumor thickness, Clark level, of ulceration, regression, tumor-infiltrating lymphocytes, mitotic rate, and the number of draining nodal basins were examined for their predictive value in SLN biopsy results. Age and thickness were analyzed as continuous variables. We did not routinely record the presence of a vertical growth phase in the primary tumor. Patients were followed up at regular intervals for recurrence and survival, and disease status was prospectively updated in the clinical database. Statistical analyses were performed with SPSS software (SPSS, Inc., Chicago, IL). Comparisons were made by using {chi}2 analysis, and estimated survival rates were calculated by the Kaplan-Meier method.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The clinicopathologic characteristics of 223 patients with thin melanoma undergoing SLN biopsy are listed in Table 1Go. Nodal metastases were found in 8 (3.6%) of 223 patients with thin melanoma who underwent SLN biopsy. Age (modeled as a continuous variable, in years), sex, location of the tumor (extremity, head and neck, or trunk), tumor thickness (modeled as a continuous variable, in millimeter measurements), Clark level, presence of ulceration, regression, tumor-infiltrating lymphocytes, mitotic rate, and number of draining nodal basins were not predictive of SLN metastases ({varepsilon}; P = not significant by {chi}2; Table 2Go).


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  		TABLE 1. Characteristics of 223 patients with thin melanoma undergoing SLN biopsy
 

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  		TABLE 2. Clinicopathologic features are not predictive of a positive sentinel lymph node biopsy
 
No evidence of nodal metastasis was found in the 73 patients with lesions <.75 mm in thickness. No positive SLN was found in 70 thin-melanoma patients with invasion to Clark level II or III. SLN metastases were found in 8 (5.3%) of 150 patients with lesions .75 to 1 mm in thickness. Eight (5.3%) of 150 patients with Clark IV lesions had positive SLNs. Among 114 highest-risk patients with thin melanomas (tumors .75–1 mm thick and invasion to Clark level IV), 8 (7%) were found to have a positive SLN (Table 3Go). It is interesting to note that among 18 patients with documented tumor ulceration, none had SLN metastases. In the patients with positive SLNs, the median number of involved nodes was 1.5. All patients with a positive SLN underwent subsequent completion lymphadenectomy; none had evidence of disease beyond the SLN(s).


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  		TABLE 3. Results of SLN biopsy in patients with thin melanoma
 
With an overall median follow-up of 25 months, there have been six patients (2.7%) with regional, in-transit, and/or systemic recurrences (Table 4Go). There were no recurrences or deaths in patients with melanoma <.75 mm in thickness. The median time to recurrence was 45 months; the median length of follow-up in the patients who experienced disease recurrence was 60 months. Of the six patients with recurrences, only one had a positive SLN at the time of diagnosis. Two of the six recurrences occurred in patients with a negative SLN biopsy but with evidence of ulceration in the primary tumor; one of these patients ultimately died of disease-related causes.


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  		TABLE 4. Recurrences in patients with thin melanoma undergoing SLN biopsy
 
The median follow-up for the eight patients with SLN metastases was 40 months (Table 5Go). Of those patients, six (75%) remain free of disease, one died of unrelated causes, and one experienced systemic disease recurrence but was alive with disease at the last follow-up. Five patients have died; of the three patients who died of melanoma, none had evidence of metastasis on SLN biopsy. Five-year disease-specific survival rates (Fig. 1Go) for patients with positive and negative SLNs are 100% and 95.7%, respectively (P = .77).


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  		TABLE 5. Outcomes in patients with thin melanoma and positive SLN biopsy
 

Figure 1
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  		FIG. 1. Disease-specific survival in patients with positive and negative sentinel lymph node (SLN) biopsy results (P = .77) for thin melanoma.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Thin melanomas are associated with an excellent prognosis, but outcomes are not uniform, and there exists a potential for recurrence and metastasis. In a recent review of a single institution’s 30-year experience with 1158 thin (<1 mm) melanomas, 6.6% of patients had advanced disease at presentation, including evidence of regional and metastatic disease. 1 With a median follow-up of 11 years, 9.4% developed recurrent disease, and disease-free survival at 20 years was reported at 59%. Published 10-year survival rates, which include patients with tumors <1.5 mm thick in some studies, range from 83% to 97.6%.2

The American Joint Committee on Cancer (AJCC) Melanoma Staging Committee analyzed >5000 thin melanomas and found that ulceration and Clark level were the factors most predictive of outcome. The 2002 AJCC staging system was constructed on incremental differences in survival based on the independent predictive values of tumor thickness, ulceration, and Clark level. The AJCC has thus effectively redefined thin melanoma as tumors ≤1 mm thick. The 10-year survival rates for thin-melanoma patients with and without ulceration are 76% and 86%, respectively. An even more powerful predictor of survival outcome was level of invasion (Clark level IV/V compared with Clark level II/III).3 However, there has been no agreement in the published literature that pathologic features associated with poorer prognosis also predict nodal metastases.

SLN biopsy for thin melanoma is advocated by some to improve staging and better predict prognosis. Currently, most surgeons offer the procedure selectively, but the clinicopathologic criteria on the basis of which patient selection is performed vary from center to center. Clear identification of high-risk thin-melanoma patients for SLN biopsy remains problematic.

Most reports in the literature are based on retrospective studies that generally include highly selected patient populations, which ultimately represent a small proportion of all those with tumors ≤1 mm. The vast majority of patients with thin melanoma do not undergo any further work-up after the initial excision. Patients with an initial diagnosis of a thin melanoma based on an incomplete excision, such as a shave biopsy, may undergo SLN biopsy at the time of definitive excision on the basis of worrisome characteristics or suspicion that a thicker lesion exists. Published incidences of positive SLN must be considered in the proper context of higher-risk patients seen at tertiary referral centers.

Our reported incidence of positive SLNs is consistent with other reports in the literature, which range from 0% to 9.7% ( Table 6Go). However, patients with risk factors such as a Clark level of IV or higher and/or .76 to 1-mm-thick melanoma have a 5% to 7% incidence of nodal metastasis. Younger age, male sex, regression, ulceration, vertical growth phase, and high mitotic rate have all been reported by various investigators as risk factors for a positive SLN biopsy.6,19–22 Others did not identify specific predictors but noted a higher incidence of nodal metastasis with increasing tumor thickness.7,15


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  		TABLE 6. SLN biopsy results in thin melanoma: a review of the literature
 
Because of inherent patient selection biases, few studies corroborate the exact findings of other similar studies. We only saw positive SLN biopsy results in patients with .75- to 1-mm-thick lesions. Although all patients with positive SLNs in our study did have Clark level IV lesions, this criterion’s value as a predictor is limited by the fact that it was the major criterion on which patient selection for the procedure itself was based. No other clinicopathologic characteristics were associated with nodal metastasis. This is not a new finding; many groups have not found reliable predictors either.15,17,23

In a report of 5480 patients with thin melanoma (≤1 mm), ulceration was seen in 6% of lesions and predicted a poorer 10-year survival when present.3 Some studies20,21 have found an association with ulceration and SLN metastases in thin melanoma, and many surgeons consider it to be an indication for SLN biopsy. Our data do not support this practice. Ulceration was seen in 18 (8.1%) of our patients, of whom none had a positive SLN. Of the six patients with recurrences, two had evidence of ulceration in the primary tumor. Thus, although ulceration, uncommonly seen in thin melanoma, portends a poorer prognosis when present, it does not seem to predict the presence of a positive SLN.

On the basis of the collective SLN experience in thin melanoma (Table 6Go), it is exceedingly uncommon to find nodal metastases in patients with very thin melanomas (≤.75 mm), even when they are seen in combination with other unfavorable clinicopathologic characteristics. Many have found no evidence of nodal metastases in this subgroup.7,8,13 Similarly, we showed that patients with very favorable thin melanomas (<.75 mm and Clark level II/III), but with other prognostic factors influencing the surgeon’s decision to perform SLN biopsy, have virtually no likelihood of nodal metastases. Some investigators6,15 report positive SLN findings in 1.7% to 2.5% of very thin melanomas; one such patient had a .35 mm Clark level II lesion, thus demonstrating that nodal metastases can occur in the absence of other poor-prognostic factors. However, we found no basis on which to recommend SLN biopsy for all thin melanomas.

Few studies report recurrence and survival data for patients with thin melanoma who undergo SLN biopsy. In this study, we showed that the risk of recurrence and death from disease was not significantly different between patients with nodal metastases and those without. This is the only study that specifically looked at outcomes of SLN biopsy patients with melanoma ≤1 mm thick. Bleicher et al.15 noted a significantly higher disease-free survival in patients with melanoma ≤1.5 mm thick and negative SLNs. As with the present study, however, the only disease-related deaths in their series were seen in patients without evidence of nodal metastasis.

Consistent with our results, Agnese et al.14 found that SLN status was not a predictor of recurrence or survival in patients with thin melanoma. With a cutoff of <1.2 mm thickness, the only recurrences seen in their series were in patients with a negative SLN biopsy. Gennari et al.7 reported disease recurrences only in patients who had negative SLN biopsies with lesions .75 to 1.5 mm thick. Both studies reported relatively short periods of follow-up, but with a favorable prognosis for thin melanomas overall, the additive value of SLN biopsy is difficult to define.

Long-term follow-up is important in thin melanoma because recurrences and disease-specific deaths are known to occur >10 years after diagnosis. The median time to recurrence for thin-melanoma patients at the Sydney Melanoma Unit is 49.8 months.2 We report a median time to recurrence of 45 months. Although our overall median follow-up is 25 months, it is 40 months in patients with a positive SLN. Although we expect to see more recurrences with longer follow-up, those who develop recurrent disease are unlikely to have had a positive SLN biopsy compared with a negative SLN biopsy. A negative SLN biopsy result in thin melanoma does not necessarily portend a more favorable outcome. In other recently reported SLN series, in which all eligible melanoma patients were included, recurrence rates for the negative-SLN group ranged from 1.7% to 11%.10,24,25

Because the group of thin-melanoma patients with positive SLN biopsy results were not at an increased risk of recurrence and death, the possibility that a therapeutic benefit was derived from SLN biopsy and completion lymphadenectomy for patients with a low risk of occult systemic disease may be considered. Given the overall excellent prognosis of thin melanoma over long periods of time, it would be premature to derive any conclusions about the effect of therapeutic lymphadenectomy in this population with such a low incidence of positive SLN biopsy results. However, patients with negative SLN biopsies who experienced disease recurrence or died without specific regional recurrences support a greater role for aggressive tumor biology in this population.

We did not see any nodal metastases in a highly selected group of patients with <.75-mm-thick lesions. The incidence of positive SLNs is 7% in patients with lesions both .75 to 1.0 mm in thickness and Clark level IV. It is reasonable to consider SLN biopsy in this group of patients, but with short-term follow-up, the prognostic implications of a positive SLN remain unclear. The significance of SLN biopsy results may be different in patients with thin melanoma than in those with intermediate-thickness tumors. Studies with longer follow-up may better assess the relevance of nodal staging in thin melanoma. Furthermore, no one has established that the risk factors for disease recurrence and death are, in fact, the same risk factors for positive SLN biopsy. Other novel methods of staging need to be pursued to more accurately identify patients at risk of recurrence.

Without vitiating the argument that the most important predictor of survival for most patients with melanoma is regional nodal status, SLN biopsy is not without risk and should not be used indiscriminately. SLN biopsy is associated with lower rates of morbidity than elective lymph node dissections, but it remains an invasive procedure with all the attendant risks of lymphatic mapping and surgery. 24,26,27


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Nodal metastasis in thin cutaneous melanoma is uncommon, especially in patients with melanoma <.75 mm thick or a Clark level less than IV. In this single-institution experience, no clinicopathologic factors were predictive of finding a positive SLN. In this series of patients with thin melanomas, a positive SLN biopsy was not associated with an adverse prognosis. Based on a low probability of positive SLNs and a lack of clear prognostic significance, the indications for SLN biopsy in patients with melanoma ≤1 mm remain to be clearly defined.

Received for publication February 22, 2005. Accepted for publication September 11, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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  13. Statius Muller MG, van Leeuwen PA, van Diest PJ, et al. No indication for performing sentinel node biopsy in melanoma patients with a Breslow thickness of less than 0.9 mm. Melanoma Res 2001; 11:303–7.[CrossRef][Medline]
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