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Annals of Surgical Oncology 9:637-645 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Multivariate Prognostic Model for Patients With Thick Cutaneous Melanoma: Importance of Sentinel Lymph Node Status

Cristina R. Ferrone, MD, Katherine S. Panageas, DrPH, Klaus Busam, MD, Mary Sue Brady, MD and Daniel G. Coit, MD

From the Departments of Surgery (CRF, MSB, DGC), Epidemiology and Biostatistics (KSP), and Pathology (KB), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Daniel G. Coit, MD, 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
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The overall prognosis of patients with thick cutaneous melanoma (TCM) is generally thought to be poor. Surgically staging these patients with sentinel lymph node (SLN) biopsy remains controversial. This study was performed to determine whether SLN status improved our ability to predict outcome over other known prognostic factors and to develop a model incorporating independent prognostic factors to estimate the risk of recurrence for an individual patient.

Methods: A prospective database identified patients with TCM (>4.0 mm or Clark level V) and clinically negative nodes who underwent SLN biopsy. Univariate and multivariate analyses were performed.

Results: From 1991 to 2001, 126 patients were identified; 75 (60%) were male. The median age was 60 years. The median tumor thickness was 5.5 mm, and 43% were ulcerated. Thirty percent of patients had a positive SLN. Recurrence was seen in 50 patients (40%). Median follow-up, relapse-free survival, and overall survival were 25, 50, and 68 months, respectively. Factors independently predictive of recurrence were age >=60 years, depth >5.5 mm, ulceration, and SLN positivity. SLN status was the most significant prognostic factor (P < .001). The relative risk of recurrence for an individual patient ranged from 1 in patients for whom no adverse factors were present to 29.4 when all factors were present.

Conclusions: SLN status was the strongest independent predictor of outcome in patients with TCM. However, patients with TCM are prognostically heterogeneous, and all independently predictive factors should be considered when an individual patient’s risk of recurrence is assessed.

Key Words: Thick cutaneous melanoma • Sentinel lymph node • Prognostic model—Recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients with localized thick cutaneous melanoma (TCM)—defined by the American Joint Committee on Cancer (AJCC) as >4 mm thick, Clark level V, or both—present a challenge for the surgeon because of their high risk of both regional and distant micrometastatic disease. In the 1980s Balch et al. examined the effect of elective regional lymph node dissection on the survival of patients with primary cutaneous melanoma.1,2 They concluded that patients with melanomas >=4 mm thick and clinically negative nodes had a high risk of both regional node metastases (>60%) and occult distant metastatic disease (>70%) at the time of initial presentation. Because this subset of patients fared poorly, with a 5-year survival of 30%, they hypothesized that aggressive locoregional management with elective lymph node dissection (ELND) was unlikely to lead to a survival benefit. They went on to suggest that ELND might provide important prognostic information in patients with TCM to help assign them onto clinical trials of adjuvant therapy. Although no contemporary prospective trials have demonstrated a survival benefit for patients with TCM undergoing routine ELND, nodal status has been repeatedly identified as a strong predictive factor of outcome. A recent study by Kim et al.,3 which considered 120 patients with TCM, found nodal status to be an independent predictor of survival. Nodal status also emerged as the strongest factor predictive of outcome in the recent review of Gershenwald et al.,4 which considered 116 patients with melanomas >=4 mm thick who underwent sentinel lymph node (SLN) biopsy (SLNB). Finally, the importance of nodal status in patients with TCM was confirmed by the AJCC5 melanoma staging committee, which recently reviewed the outcome of 1380 patients with primary tumors >4 mm, without clinical evidence of nodal metastases at presentation, whose nodes were pathologically staged by either SLNB or elective lymphadenectomy. Nodal status again emerged as the most significant predictor of outcome.

The prognostic heterogeneity of these patients is further reflected in the history of their ambivalent AJCC stage group assignment. Over the last 15 years, these patients have migrated from AJCC stage IIB6 (in 1983), to III7 (1988), to IIB8 (1992), to III9 (1997). Most recently, the AJCC has proposed to change the stage group assignment of patients with TCM back to IIB,10 acknowledging their prognostic diversity but maintaining the concept of stage III as reflecting regional metastatic disease.

However, nodal status alone is insufficient to assess prognosis in patients with TCM. Other factors, such as increasing tumor thickness, primary tumor ulceration, patient age and sex, and tumor location have been shown to affect outcome. Survival varies widely (30%–80% at 5 years) depending on the status of these prognostic factors.1,3,4,5 The biological complexity of this group of patients, whose prognosis seems to be governed by multiple factors, may exceed the ability of a simple, clinically useful, intuitive staging system to be prognostically accurate. This would justify an effort to develop a prognostic model incorporating all factors predictive of outcome to assign a risk of recurrence to individual patients, independently of a more conventional staging system.

The first aim of this study was to define the clinical and pathologic factors predictive of outcome in patients with TCM from a single center, who were treated consistently in this contemporary era of SLNB. The second aim was to incorporate the important independent prognostic factors derived from the entire group into a predictive clinical model to develop a relative risk (RR) profile that might apply to the individual patient.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
A prospective computerized surgical melanoma database including all patients undergoing SLNB at Memorial Sloan-Kettering Cancer Center was reviewed to determine relevant clinical information and to identify dates of recurrence or death. Between 1991 and 2001, we identified 126 patients with TCM who met the criteria. Of these 126 patients, 16 were previously reported by Kim et al.3 TCM was strictly defined according to the AJCC definition of T4: melanomas >4 mm thick, Clark level V, or both. Known prognostic factors were documented for each patient, including age, sex, tumor thickness, Clark level, location, presence of ulceration, and pathologic status of the SLN. Before SLNB, all patients had clinically negative nodes and no evidence of distant disease on the basis of physical examination and appropriate radiological studies (chest x-ray, computed tomography, magnetic resonance imaging, positron emission tomography, or a combination of these).

SLN Mapping Technique
Patients underwent lymphatic mapping and SLNB as has been previously described.11 Lymphoscintigraphy with intradermally administered 99mTc-labeled sulfur colloid established the lymphatic drainage patterns to identify SLNs within basins at the highest risk for metastatic melanoma. Intradermal blue dye injection was performed during surgery around the intact tumor or biopsy site. The SLN was defined as the blue node, the hottest node of all the nodes, or any node containing >10% radioactivity of the hottest node counts ex vivo. All SLNs were excised and submitted for pathologic review. Earlier SLN specimens were analyzed by conventional hematoxylin and eosin (H&E) staining. More recent specimens were evaluated by H&E, and if they were negative by H&E, immunohistochemical staining with S100 and HMB-45 was performed. Primary tumors were excised with >=2-cm margins as appropriate for tumor thickness.

Patients did not routinely receive adjuvant therapy, because no standard treatment was available during the study period. However, patients were offered participation in prospective clinical trials to evaluate innovative immunotherapy strategies.

Statistical Analysis
Relapse-free survival (RFS) and overall survival (OS) were calculated from the date of surgery of the primary melanoma and SLNB to the date of initial recurrence, death, or last follow-up. Survival distributions were estimated by the Kaplan-Meier method and compared by use of the log-rank test. Multivariate analysis was performed with the Cox proportional hazard model. Parameter estimates from this multivariate model were used to obtain RR of recurrence.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Characteristics
Clinical and pathologic characteristics are listed in Table 1. The median age was 60 years (range, 15–90 years), and 60% were male. The median and mean tumor thicknesses were 5.5 and 6.7 mm, respectively (range, 1.8–24 mm). Ulceration was seen in 43%. Tumors were axial, including trunk and head and neck, in 55%, and were in an extremity location in 45%.


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  		TABLE 1. Clinical and pathologic factors of 126 patients with TCM
 
SLN Status
At least 1 SLN was identified in all 126 patients. The median number of SLNs collected was 2 (range, 1–3). Of 126 patients, 38 (30%) had at least 1 positive SLN. All patients who had a positive SLN underwent completion lymphadenectomy. Eight (21%) of 38 patients had at least 1 positive non-SLN.

Adjuvant Therapy
Thirteen patients received adjuvant therapy after surgery of their primary melanoma. Of these 13 patients, SLNs were positive in 7 and negative in 6. Two patients received high-dose interferon, and 11 were entered onto vaccine trials. Of the two patients who received interferon, one had a positive SLN and one had a negative SLN. Five of the patients who participated in the vaccine trial had recurrences (four systemic and one local). Two patients who received high-dose interferon and four patients who received vaccines had not had recurrence at the time of last follow-up.

Follow-Up
Complete follow-up data were available for all 126 patients. The mean follow-up was 25 months. The median follow-up was 16 months (range, .7–122 months). For patients who had not had disease recurrence at the time of last follow-up, the mean and median follow-up were 31 and 27 months, respectively. For patients who had recurrence at the time of last follow-up, the mean and median follow-up were 16 and 10 months, respectively.

At last follow-up, 76 (60%) of 126 patients had remained continuously free of disease, and 50 (40%) had experienced a recurrence. Of those 50 patients who had a recurrence, 32 (64%) are dead of disease, 11 (22%) are alive with disease, and 7 (14%) were rendered free of disease after a subsequent surgical intervention.

Outcome
OS and RFS for the entire group are shown in Fig. 1. The average interval from relapse to death was 24 months. Most events had occurred by 60 months after surgery. Because relapse seems to be an early surrogate for outcome in these patients, we used RFS as the primary end point for subsequent analysis.



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  		FIG. 1. Kaplan-Meier overall and disease-free survival for patients undergoing successful lymphatic mapping and sentinel lymph node biopsy (n = 126). The median relapse-free and overall survival were 50 and 68 months, respectively. The 3-year relapse-free and overall survivals were 56% and 76%, respectively. Five-year relapse-free and overall survivals were 48% and 63%, respectively.

 
On univariate analysis (Table 2), age (<60 and >=60 years), tumor thickness (<=5.5 and >5.5 mm), ulceration (present and absent), and SLN status (positive and negative) were all statistically significant prognostic factors. Age and tumor thickness thresholds were based on the median. Survival distributions reflecting the presence or absence of these factors are shown in Fig. 2A through 2D. Age <60 years, thickness <=5.5 mm, absence of ulceration, and a negative SLN were all favorable predictors. On multivariate analysis (Table 3), all four factors remained statistically significant prognostic factors. Of these four factors, SLN status emerged as the strongest independent predictor of outcome (P < .001).


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  		TABLE 2. Univariate factors predictive of recurrence
 


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  		FIG. 2. Kaplan-Meier relapse-free survival (RFS) distributions reflecting the presence or absence of significant prognostic factors. (A) The 5-year RFS for patients <60 years old (n = 58) and >=60 years (n = 68) with thick cutaneous melanoma (TCM) was 64% and 30%, respectively (P = .003). (B) The 5-year RFS for patients with melanomas <=5.5 mm thick (n = 66) and >5.5 mm thick (n = 60) was 61% and 31%, respectively (P = .002). (C) The 5-year RFS for patients with a nonulcerated TCM (n = 72) and an ulcerated TCM (n = 54) was 66% and 32%, respectively (P = .002). (D) The 5-year RFS for patients with TCM and a negative SLN (n = 88) or a positive SLN (n = 38) was 56% and 32%, respectively (P = .0008).

 

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  		TABLE 3. Multivariate factors predictive of recurrence
 
Prognostic Model
In an effort to incorporate all four independent factors into a prognostic model, we first looked at outcome by the number of adverse factors present (Fig. 3). Low-, intermediate-, and high-risk groups were defined according to the number of factors present. The low-risk group (n = 16), with no adverse factors present, had a 5-year RFS of 84%. The high-risk group (n = 7), with all four adverse factors present, had a median survival of 6 months; all of these patients had relapsed by 18 months. For the majority, the intermediate-risk group (n = 103), one to three factors were present. These patients have a median survival of 43 months and an RFS of 45% at 5 years.



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  		FIG. 3. Kaplan-Meier relapse-free survival (RFS) for low-, intermediate-, and high-risk groups based on the number of adverse prognostic factors present. For the low-risk group (n = 16), with no adverse factors present, the RFS at 5 years was 84%. The intermediate-risk group (n = 103), with one to three factors present, had a 45% 5-year RFS. The high-risk group (n = 7), with all four factors present, had a 0% RFS beyond 18 months. RFS was significantly better for patients in the low-risk group as compared with the intermediate-risk group (P = .02) and in the intermediate-risk group compared with the high-risk group (P <= .0001).

 
This first model assigns equal importance to each of the four factors. However, the multivariate analysis would suggest that each prognostic factor confers a different degree of risk. On the basis of this observation, and in an attempt to develop a more accurate RR assessment, a mathematical model was created in which each prognostic factor is assigned a relative weight proportional to its statistical power. This model can be expressed in the following equation:


(1)

This equation allows us to assign each patient a number equivalent to his or her RR of recurrence, on the basis of the individual contribution of each of the four independent risk factors. If the factor is absent (i.e., age <60 years, thickness <=5.5 mm, absence of ulceration, or a negative SLN), a value of 0 is assigned for that portion of the equation, whereas if the factor is present a value of 1 is assigned. Therefore, if all four factors are absent, the exponential of 0 equals an RR of 1. This group corresponds to the low-risk group shown in Fig. 3. When all four factors are present, the RR equals 29.4, corresponding to the high-risk group in Fig. 3. An example of the intermediate group would be a patient who is 55 years old and has a 6-mm nonulcerated primary tumor and a positive SLN; RR of recurrence is calculated to be 6 (i.e., six times that of a patient with no risk factors). As seen in Fig. 4, the intermediate-risk group can be further subdivided into a low/intermediate- and a high/intermediate-risk group. The low/intermediate-risk group (n = 34; RR, 1.1–4.9) had a 5-year RFS of 73%, compared with the 5-year RFS of 28% in the high/intermediate-risk group (n = 69; RR, 5–29; P = .002).



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  		FIG. 4. Kaplan-Meier relapse-free survival (RFS) based on the relative risk (RR) equation. An RR of 1 and 29 corresponds to the low- and high-risk groups, respectively, in Fig. 3. The intermediate-risk group is further stratified on the basis of the RR equation. The low/intermediate-risk group (RR, 1–5; n = 34) had a median of 66 months and a 5-year RFS of 73%. The high/intermediate-risk group (RR 5–28.9; n = 69) had a median of 31 months and a 5-year RFS of 28%. RFS was significantly better in the low/intermediate-risk group as compared with the high/intermediate-risk group (P = .002) and in the high/intermediate-risk group compared with the high-risk group (P <= .001). There was no statistical difference between the low-risk and the low/intermediate-risk group (P = .3).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Patients who present with clinically localized TCM present a challenge for the surgeon because of their high risk of regional and distant micrometastatic disease. Despite this, these patients do not all fare poorly. They are more prognostically diverse than any other group of melanoma patients and have defied simple classification, as is reflected in their lack of a permanent "home" in the AJCC staging system since its inception in 1977.

Earlier studies consistently identified nodal status and increasing thickness as factors predictive of recurrence (Table 4). Despite the consistency of these prognostic factors in patients with TCM, the reported 5-year RFS has ranged from 13% to 59%. Whereas many patients in early studies underwent ELND, more recently SLNB has been used to surgically stage patients with TCM. The study of Gershenwald et al.4 and our study both evaluated the role of SLN status in patients with TCM. The frequency of a positive SLN (30% vs. 39%) and 3-year RFS (76% vs. 72%) were quite comparable in these two contemporary studies. Both studies conclude that SLN status is the strongest prognostic factor of outcome for patients with TCM.


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  		TABLE 4. Reported experiences of patients with TCM
 
The importance of SLN staging was recently acknowledged by the changes incorporated into the new AJCC melanoma staging system. The proposed revisions of the AJCC staging system have recognized the two most consistent prognostic factors in patients with localized melanoma to be SLN status and ulceration. The committee has recommended surgical staging of regional lymph nodes with SLNB, where available, and has incorporated ulceration into the definition of T stage. Inevitably, however, as more factors are incorporated into any staging system, although the system may become more prognostically accurate, it becomes more cumbersome and difficult to use, particularly for those who do not deal with the disease on a daily basis.

The method of developing a prognostic model may represent an improvement over conventional staging systems. It is designed to incorporate not just a few, but all factors known to be independently predictive of outcome to develop an RR profile for the individual patient. This model is able to segregate patients into groups with similar risks of recurrence, regardless of the factors that led to that risk. The TCM patients evaluated in this study are all staged as clinical stage III by the current AJCC7 system, yet their RFS in patient subsets ranges from 0% to 85% at 5 years. The first prognostic model developed in this study (Fig. 3) attempts to separate these patients into three smaller and more homogeneous groups on the basis of the number of prognostic factors that are present. The four factors that emerged as independent predictors of recurrence were age, thickness, ulceration, and SLN status. By assigning equal prognostic weight to each of these factors, patients can be separated into a low-risk (no factors present), intermediate-risk (one to three factors present), or high-risk (all four factors are present) group to predict their RFS. The advantage of this model is its ease of use. This model, however, segregates out only small subsets of patients who will do very well or very poorly, leaving a large intermediate-risk group.

The second prognostic model developed is more complex but potentially more accurate. The model is able to further divide the large intermediate-risk group into low/intermediate- and high/intermediate-risk groups. The low/intermediate- and high/intermediate-risk groups developed by this model continue to demonstrate the significant heterogeneity in the original intermediate-risk group, with 5-year RFS ranging from 28% to 73%. The definition of these more homogeneous groups, especially in this high-risk cohort of TCM patients, may be extremely important as we design clinical trials to evaluate the effect of adjuvant therapy in cohorts of patients with uniform prognosis.

The concept of a mathematical model has several disadvantages. The first is its inherent complexity. The clinician cannot be expected to recall the equation or to perform the necessary calculations. Rather, it should be used to develop prognostic nomograms, which could be carried in the clinics both to counsel the patients and to assess them for entry onto trials. Furthermore, accurate prognostic nomograms must be based on many more observations with longer follow-up to narrow the confidence intervals of their predictions. Optimally, such nomograms could be developed for all patients with localized malignant melanoma, rather than the arbitrary subset of patients with TCM. Nomograms would then recognize the multiple intersecting biological continua that ultimately govern prognosis in these patients.

In conclusion, patients with TCM represent a heterogeneous group of patients whose outcome cannot be predicted by tumor thickness alone. In this analysis, SLN status has again emerged as the single most important predictor of outcome. A prognostic model has been presented that considers all four independent prognostic factors: age, thickness, ulceration, and SLN status. Considering all factors together may allow patients to be staged and stratified more accurately, compared with a traditional staging system. Separating patients into groups with a more uniform prognosis will be extremely important for future clinical trials designed to evaluate the effect of adjuvant therapy.


   Acknowledgments
 
The authors thank Javier Betancourt for his assistance with the patient database.


   Footnotes
 
Patients with thick cutaneous melanoma are prognostically heterogeneous, and all independently predictive factors, including sentinel lymph node status, primary tumor thickness and ulceration, and patient age, should be considered when an individual patient's risk of recurrence is estimated.

Received for publication February 27, 2002. Accepted for publication May 14, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Balch CM. Surgical management of regional lymph nodes in cutaneous melanoma. J Am Acad Dermatol 1980; 3: 511–24.[Medline]
  2. Balch CM, Soong SJ, Milton G, et al. A comparison of prognostic factors and surgical results in 1,786 patients with localized (stage I) melanoma treated in Alabama, USA, and New South Wales, Australia. Ann Surg 1982; 196: 677–84.[Medline]
  3. Kim S, Garcia C, Rodriguez J, Coit D. Prognosis of thick cutaneous melanoma. J Am Coll Surg 1999; 188: 241–7.[CrossRef][Medline]
  4. Gershenwald JE, Mansfield PF, Lee JE, Ross MI. Role for lymphatic mapping and sentinel lymph node biopsy in patients with thick (>=4 mm) primary melanoma. Ann Surg Oncol 2000; 7: 160–5.[Abstract]
  5. Balch CM, Soong SJ, Gershenwald JE, et al. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol 2001; 19: 3622–34.[Abstract/Free Full Text]
  6. Beahrs OH, Meyers MH, eds. Manual for Staging of Cancer: American Joint Committee on Cancer. 2nd ed. Philadelphia: Lippincott, 1983.
  7. Beahrs OH, Henson DE, Hutter RVP, Myers MH, eds. Manual for Staging of Cancer: American Joint Committee on Cancer. 3rd ed. Philadelphia: Lippincott, 1988.
  8. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ, eds. Manual for Staging of Cancer: American Joint Committee on Cancer. 4th ed. Philadelphia: Lippincott, 1992.
  9. Fleming ID, Cooper JS, Henson DE, et al., eds. Manual for Staging of Cancer: American Joint Committee on Cancer. 5th ed. Philadelphia: Lippincott-Raven, 1997.
  10. Balch CM, Buzaid AC, Soong SJ, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 2001; 19: 3635–48.[Abstract/Free Full Text]
  11. Coit DG. How we do it: the Memorial Sloan-Kettering Cancer Center approach.In: Cody HSIII, ed. Sentinel Lymph Node Biopsy. London: Martin Dunitz, 2002: 135–42.
  12. Coit D, Sauven P, Brennan M. Prognosis of thick cutaneous melanoma of the trunk and extremity. Arch Surg 1990; 125: 322–6.[Abstract]
  13. Sylaidis P, Gordon D, Rigby H, Kenealy J. Follow-up requirements for thick cutaneous melanoma. Br J Plast Surg 1997; 50: 349–53.[CrossRef][Medline]



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