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Annals of Surgical Oncology 9:975-981 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Prognostic Importance of Lymph Node Tumor Burden in Melanoma Patients Staged by Sentinel Node Biopsy

Jaime M. Ranieri, MD, Jeffrey D. Wagner, MD, Rafael Azuaje, MD, D. Davidson, MD, Stacie Wenck, RN, Joanne Fyffe, MS and John J. Coleman, III, MD

From the Departments of Surgery/Plastic and Reconstructive Surgery (JMR, JDW, RA, SW, JJC), Pathology (DD), and Medicine/Biostatistics (JF), Indiana University School of Medicine, Indiana University-Purdue University, Indianapolis, Indiana.

Correspondence: Address correspondence and reprint requests to: Jeffrey D. Wagner, MD, RT 471, Cancer Pavilion, 535 Barnhill Dr., Indianapolis, IN 46202; Fax: 317-278-3164; E-mail: jdwagner{at}iupui.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: The objective of this study was to investigate the relationship between nodal tumor burden and the outcomes of recurrence and survival in sentinel node–positive melanoma patients.

Methods: We reviewed a series of sentinel node–positive patients with primary cutaneous melanoma treated with completion lymph node dissection (CLND). Microscopic nodal tumor deposits were counted and measured with an ocular micrometer. Various measures of tumor burden and traditional melanoma prognostic indicators were studied in multivariate Cox regression models.

Results: Sentinel lymph node and CLND specimens were evaluated in 90 node-positive patients. The diameter of the largest lymph node tumor nodule and the total lymph node tumor volume were significant predictors of recurrence (two-sided P < .0001 for both) and survival (two-sided P = .0018 and P = .0002, respectively). A tumor deposit diameter of 3 mm was identified as the most significant cut point predictive of recurrence (P < .0001; hazard ratio, 5.18) and survival (P < .0001; hazard ratio, 5.43). The 3-year survival probability was .86 for patients with largest tumor deposit diameters of <=3 mm and was .27 for patients with largest deposit diameters >3 mm (P < .0001).

Conclusions: Microstaging of melanoma sentinel lymph node/CLND specimens by using the diameter of the largest tumor deposit is a highly significant predictor of early relapse and survival.

Key Words: Melanoma • Metastasis • Nodal tumor burden • Lymph nodes


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
The presentation of American Joint Committee on Cancer stage III melanoma1 has changed dramatically since the introduction of sentinel lymph node (SLN) biopsy for nodal staging by Morton et al.2 in 1992. SLN biopsy is now standard practice in most major medical centers for staging regional lymph nodes in patients with cutaneous melanoma. Most stage III melanomas are now detected with microscopically positive nodes rather than clinically palpable nodes. The 5-year survival rates for stage III melanoma range from 13% to 69%, depending on the burden of nodal disease and the presence of ulceration.3 The histological status of the sentinel node has been reported to be a more important prognostic factor than tumor thickness in patients with clinically localized regional disease.4 Sentinel node biopsy (SNB) permits enhanced pathologic analysis of one or two lymph nodes. Step sections and immunohistochemical techniques often identify microscopic nodal metastases <.1 mm in diameter.5

The American Joint Committee on Cancer recently modified the staging system for cutaneous melanoma.1 Stage III subsets were previously based on the size of the nodal metastases and the presence of in-transit metastases. Recent data show the number of metastatic lymph nodes, gross differences in nodal tumor burden (i.e., clinically occult [detected pathologically] vs. clinically apparent [macroscopic, detected by clinical examination]), and the presence of ulceration of the primary tumor to be the most important prognostic variables in stage III melanoma.3 SNB permits more precise measurements of smaller tumor burdens in clinically "normal" lymph nodes. We hypothesized that it may be possible to further substratify stage III patients by quantifying the microscopic metastatic tumor burden within the regional lymph node basin.

The objective of this study was to investigate the relationship between the regional lymph node tumor burden and the outcomes of recurrence and survival in patients with clinically localized melanoma staged by SLN biopsy and selective lymphadenectomy for identification of occult nodal metastases.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Patients
The Indiana University Interdisciplinary Melanoma Program computerized database was queried to retrospectively identify consecutive patients who underwent a SLN biopsy for clinically localized melanoma at Indiana University Medical Center and affiliated hospitals between 1994 and 2000. All patients with a positive SNB were identified. Patient demographics, primary tumor thickness, location of primary tumor, presence of tumor ulceration, number of lymph nodes removed, pathology of examined nodes, and number of lymph nodes involved with tumor were recorded. Disease status and dates of last clinical contact were determined. Archived lymph node slides and blocks for these selected patients were analyzed for microscopic tumor burden determination.

During the time period covered by the study, SNB indications were in evolution. Initially, SNB was offered as a nodal staging procedure to patients with clinically localized, intermediate-thickness melanoma (1–4 mm). As experience with the procedure grew, indications were liberalized to include patients with melanomas <1 mm and >4 mm deep.

Methods
Intraoperative SNB
In general, SNB was performed with vital blue dye and radiolocalization together to ensure complete removal of all sentinel nodes, by using the technique previously described.6,7 Briefly, preoperative dynamic dermatolymphoscintigraphy was used to identify the basin(s) at risk for lymph node disease. One to two millicuries of 99mTc-labeled sulfur colloid was injected intradermally at the tumor site 2 to 4 hours before surgery. Continuous imaging with a large field of view gamma camera for up to 2.5 hours was then performed, depending on the location of the primary melanoma. The first node(s) in each basin to accumulate radiotracer and nodes with an observed lymphatic channel from the site of injection were marked on the skin. After the induction of anesthesia, .5 to 2.0 mL of isosulfan blue dye (LymphazurinTM; Zenith Parenterals, Rosemont, IL) was injected intradermally around the site of the primary melanoma. Those basins identified by lymphoscintigraphy were explored through limited incisions guided by the use of a handheld gamma probe (C-TrackTM; Care Wise Medical Products, Morgan Hill, CA). All blue nodes were identified and removed as sentinel nodes. The most radioactive blue SLN was then compared with the residual lymph node basin radioactivity, and, if necessary, additional radioactive nodes were removed until the ratio of the most radioactive ex vivo sentinel node to that of the residual basin was at least 10:1. If frozen- or permanent-section analysis revealed metastatic melanoma in the SLN(s), a completion lymph node dissection (CLND) was performed. Sentinel node–negative patients were generally observed without further lymph node surgery.

Histological Analysis of Surgical Specimens
At the discretion of the surgeon, suspicious sentinel nodes were sometimes submitted for frozen-section analysis. Nonsuspicious and frozen section–negative sentinel node(s) were fixed in formalin, submitted for 1-mm step sections, and analyzed by hematoxylin and eosin stains. Sentinel nodes negative for metastases were then subjected to further analysis with S-100 and/or HMB-45 immunostains (at least one level per sentinel node). If necessary, frozen section–positive nodes were recut for additional sections to determine maximum tumor nodule diameters for tumor volume estimation. Non-SLNs and nodes from lymph node dissection specimens were analyzed in routine fashion after formalin fixation, with one to three sections from each node being reserved for hematoxylin and eosin staining.

Determination of Lymph Node Tumor Burden
Aggregate nodal tumor volumes were calculated from archived slides and blocks. Individual tumor deposits within positive nodes were identified. An ocular micrometer was used to estimate the maximum diameters of individual tumor deposits within each node. Volumes of individual tumor deposits were calculated as spheres by using the largest deposit radius with the following equation: volume deposit = 4/3 x {pi} (deposit radius)3. Aggregate tumor volumes for sentinel and nonsentinel nodes were calculated by summing the volumes of individual deposits. The total aggregate volume for each nodal basin containing tumor was calculated by summing the volumes of all tumor-containing lymph nodes in the basin.

Statistical Analysis
Spearman correlation coefficients were calculated for continuous variables, including tumor thickness, Clark’s level of invasion, patient’s age, tumor volume of the SLN, tumor volume of the CLND, total tumor volume, number of tumor deposits, number of basins, total number of positive nodes, and cross-sectional diameter of the single largest tumor deposit. The Student’s t-test and the Wilcoxon rank-sum test were used to test means and medians, respectively, between groups. Univariate analysis with Cox’s proportional hazards regression model was used for each of the prognostic factors. Multivariate analysis was performed with the same prognostic factors, with either total calculated tumor volume or the largest cross-sectional diameter used as a predictor, because these variables were not independent. In addition, multivariate analysis was also performed with a dichotomized tumor volume and diameter. When tumor volume was analyzed as a continuous variable, a log transformation was first applied to correct for skewness of the data. The values in the transformed scale were in a more normal distribution than the original scale. To determine the best cutoff values for deposit diameter and tumor volume, the Wald {chi}2 statistic was calculated for several values while adjusting for covariates to determine at which value the statistic was maximized.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Four hundred sixty-one patients with clinically node-negative cutaneous melanoma underwent SLN biopsy between February 1994 and December 2000. Ninety patients (19.5%) had a positive SLN procedure. Additional metastatic disease was discovered in the non-SLNs in 13 patients (14%). The mean age of the study population was 51.2 years (range, 14 to 88 years). There were 53 male patients (59%) and 37 female patients (41%) in the study group. The mean Breslow thickness was 3.48 mm (range, .60 to 16 mm). Histological ulceration was noted in 37.8% of patients.

The mean number of tumor-positive nodes was 1.42 (range, 1–5). The mean number of tumor deposits was 3.93 (range, 1–18). The median sentinel node tumor volume was .49 mm3 (range, .0005–12,638 mm3; mean, 576 mm3). The mean diameter of the largest single tumor deposit was 3.14 mm (range, .10–28.9 mm). The largest tumor deposit was found to correlate with tumor thickness (r = .30; P = .004), tumor volume of the sentinel node (r = .98; P < .0001), total tumor volume of the regional basin (r = .99; P < .001), and the total number of positive nodes (r = .21; P = .04).

Univariate analyses of time to recurrence and overall survival to several patient, primary tumor, and nodal tumor burden variables are listed in Table 1. By univariate analysis, the largest cross-sectional diameter of tumor deposit was a statistically significant predictor of time to recurrence and overall survival (two-sided P < .0001 and P = .0045, respectively). The tumor volume of the SLN and the total tumor volume (SLN plus CLND) were associated with time to recurrence (two sided; both P < .0001) and survival (two-sided P = .0002 and P = .0003, respectively).


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  		TABLE 1. Univariate analysis of clinical variables to recurrence and survival
 
Multivariate analysis was conducted with all prognostic factors, and those factors with a P value <=.20 were selected into the final model. Tumor volume and the largest cross-sectional deposit diameter were selected into the final model; other variables failed to show independent prognostic importance in the proportional hazard regression. The largest cross-sectional tumor deposit diameter was modeled in the multivariate analysis as a continuous variable and with dichotomous cut points of 1 and 3 mm. For survival, these cut-point values were derived by calculating the Wald {chi}2 statistic for several values with age as a covariate to determine at which value the statistic was maximized (Fig. 1, A and B). For recurrence, Breslow was kept in the model as a covariate.



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  		FIG. 1. (A) Comparison of possible tumor diameter cut points with multivariate analysis of recurrence. (B) Comparison of possible tumor diameter cut points with multivariate survival analysis.

 
Multivariate modeling showed that the total tumor volume (SLN plus CLND) and the diameter of the largest tumor deposit were significant predictors of recurrence (Tables 2 and 3) and survival (Tables 4 and 5). A tumor deposit diameter of 3 mm was identified as the most significant cut point predictive of recurrence (P < .0001) and survival (P < .0001) (Tables 6 and 7). When the largest cross-sectional diameter of tumor deposit was included in multivariate models, sex, age, tumor thickness, ulceration, location, number of tumor deposits, and number of positive nodes were not significant predictors of outcome (Table 8).


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  		TABLE 2. Final multivariate model of recurrence with continuous tumor volume
 

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  		TABLE 4. Final multivariate survival model with continuous tumor volume
 

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  		TABLE 6. Final multivariate model of recurrence (dichotomized tumor diameter >3 mm)
 

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  		TABLE 8. Multivariate analysis of largest tumor deposit diameter (continuous) to recurrence and survival
 

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  		TABLE 3. Final multivariate model of recurrence with continuous diameter
 

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  		TABLE 5. Final multivariate survival model with continuous diameter
 

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  		TABLE 7. Final multivariate survival model (dichotomized tumor diameter >3 mm)
 
At a median clinical follow-up of 37.6 months, 36 patients (40%) had disease recurrence, and 27 patients (30%) died. The largest tumor deposit diameter was a highly significant prognostic factor associated with recurrence and survival. The 3-year probability of no recurrence was .74 for patients with the largest deposit diameter <=3 mm and was .16 for patients with the largest deposit diameter >3 mm (P < .0001) (Fig. 2). The 3-year survival probability was .86 for patients with largest deposit diameters <=3 mm and was .27 for patients with the largest deposit diameters >3 mm (P < .0001) (Fig. 3).



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  		FIG. 2. Recurrence by diameter of the largest lymph node tumor deposit.

 


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  		FIG. 3. Survival by diameter of the largest lymph node tumor deposit.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
Recent studies have shown the number of metastatic nodes to be the most powerful predictor of outcome in patients with stage III melanoma. A recent multicenter analysis confirmed this finding, as well as the additional findings that the tumor burden at the time of staging (i.e., microscopic versus macroscopic) and the presence or absence of ulceration of the primary melanoma are also significant predictors of outcome.3 These findings form the basis of the recent changes instituted in the 2002 American Joint Committee on Cancer staging system for cutaneous melanoma.1

Although the size of grossly involved lymph nodes is not a particularly useful prognostic feature,8–11 the relevance of microscopic tumor burden as a prognostic indicator has only recently been investigated in the- modern era of SNB. The subclinical (generally microscopic) regional nodal tumor burdens typically encountered in patients staged by SNB have been previously described.6 In this study, we investigated the relationship between the regional lymph node tumor burden and the outcomes of recurrence and survival in patients staged by SNB.

Our data indicate the diameter of the largest nodal tumor deposit to be a significant predictor of recurrence and survival, with a tumor deposit of 3 mm identified as the most significant cut point. Tumor volume calculated as a function of deposit radius was also prognostically significant in predicting recurrence and survival. Metastatic tumor volumes typically noted were extremely small, and despite conscientious measurements, calculated tumor volumes must be considered estimates.6 In addition, deposit volumes were calculated as spheres because most deposits approximated this shape. However, there is considerable diversity in the shapes of tumor deposits. The largest deposit diameter is easily measured and is more reproducible.

Our findings confirm previous reports showing that most of the metastatic tumor burden is confined to the sentinel nodes.6,7 This probably explains why the tumor volume of the CLND alone was not a significant predictor of recurrence or overall survival (P = .20 and P = .13, respectively). The tumor volume of the SLN and the combined tumor volume of the SLN and CLND were significant predictors of recurrence (both P < .0001) and survival (P = .0002 and P = .0003, respectively). These findings may also be attributed to the small number of patients with positive nonsentinel nodes. In most patients, the largest tumor deposit was located in the sentinel node. This suggests that the most important prognostic indicators (i.e., the largest nodal deposit diameter) can generally be obtained from SNB alone and that CLND may not provide much additional prognostic information.

It is known that standard pathologic analysis of SLNs identifies only approximately 70% of melanoma metastases12 and that most of the tumor burden lies within the SLN(s).6,7 Many major melanoma centers have adopted protocols that include step-sectioning and immunohistochemical analysis to ensure that small tumor deposits will not be overlooked. With this degree of histopathologic scrutiny of SLNs, the estimation of the largest tumor deposit diameter is a relatively simple maneuver. The addition of nodal tumor deposit diameter may provide further prognostic stratification of the heterogenous stage III melanoma group. Such prognostic categories may assist in selecting patients who may benefit from adjuvant therapy or entrance onto clinical trials.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Microstaging of tumor burden in sentinel lymphadenectomy specimens by using the diameter of the largest tumor deposit provides a highly significant predictor of outcome in stage III melanoma patients. Relatively small increases in the burden of regional nodal disease correlate negatively with time to relapse and survival. These findings may permit further substratification of patients with American Joint Committee on Cancer node-positive disease.


   Footnotes
 
Microstaging of tumor burden in sentinel lymphadenectomy specimens by using the diameter of the largest tumor deposit provides a highly significant predictor of outcome in stage III melanoma patients. Relatively small increases in the burden of regional nodal disease correlate negatively with time to relapse and survival.

Received for publication March 22, 2002. Accepted for publication August 19, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

  1. Balch CM, Buzaid AC, Soong S-J, 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]
  2. Morton DL, Wen DR, Wong JH, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 1992; 127: 392–9.[Abstract]
  3. Balch CM, Soong S-J, 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]
  4. Gershenwald JE, Thompson W, Mansfield PF, et al. Multi-institutional melanoma lymphatic mapping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. J Clin Oncol 1999; 17: 976–83.[Abstract/Free Full Text]
  5. Yu LL, Flotte TJ, Tanabe KK, et al. Detection of microscopic melanoma metastases in sentinel lymph nodes. Cancer 1999; 86: 617–27.[CrossRef][Medline]
  6. Wagner JD, Davidson D, Coleman JJ III, et al. Lymph node tumor volumes in patients undergoing sentinel lymph node biopsy for cutaneous melanoma. Ann Surg Oncol 1999; 6: 398–404.[Abstract]
  7. Wagner JD, Gordon MS, Chuang T-Y, et al. Predicting sentinel and residual lymph node basin disease after sentinel lymph node biopsy for melanoma. Cancer 2000; 89: 453–62.[CrossRef][Medline]
  8. Bevilacqua RG, Coit DG, Rogatko A, Younes RN, Brennan MF. Axillary dissection in melanoma: prognostic variables in node-positive patients. Ann Surg 1990; 212: 125–31.[Medline]
  9. Coit DG, Rogatko A, Brennan MF. Prognostic factors in patients with melanoma metastatic to axillary or inguinal lymph nodes. A multivariate analysis. Ann Surg 1991; 214: 627–36.[Medline]
  10. Drepper H, Biess B, Hofherr B, et al. The prognosis of patients with stage III melanoma. Prospective long-term study of 286 patients of the Fachklinik Hornheide. Cancer 1993; 71: 1239–46.[CrossRef][Medline]
  11. Buzaid AC, Tinoco LA, Jendiroba D, et al. Prognostic value of size of lymph node metastases in patients with cutaneous melanoma. J Clin Oncol 1995; 13: 2361–8.[Abstract/Free Full Text]
  12. Joseph E, Brobeil A, Glass F, et al. Results of complete lymph node dissection in 83 patients with positive sentinel nodes. Ann Surg Oncol 1998; 5: 119–25.[Abstract]



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