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10.1245/s10434-006-9223-5
Annals of Surgical Oncology 14:1014-1019 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Evaluation of Three Scoring Systems Predicting Non Sentinel Node Metastasis in Breast Cancer Patients with a Positive Sentinel Node Biopsy

Christine E. Dauphine1, Jason S. Haukoos2,3, Maria P. Vargas1, Nova M. Isaac1, Iraj Khalkhali4 and Hernan I. Vargas1

1 Department of Surgery, Harbor-UCLA Medical Center, Torrance, California, USA
2 Department of Emergency Medicine, Denver Health Medical Center, Denver, Colorado, USA
3 Department of Preventive Medicine and Biometrics, University of Colorado Health Sciences Center, Denver, Colorado, USA
4 Department of Radiology, Harbor-UCLA Medical Center, Torrance, California, USA

Correspondence: Address correspondence and reprint requests to: Hernan I. Vargas; Section of Surgical Oncology, 1000 West Carson Street, Box 25, Torrance, CA 90502, USA; E-mail: hvargas{at}ucla.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: Completion axillary lymph node dissection (cALND), performed after a positive sentinel lymph node biopsy (SLNB) in breast cancer patients, often results in no additional positive nodes. Scoring systems have been published to aid in the prediction of nonsentinel node metastasis. Our purpose was to assess the validity of these scoring systems in our patient population.

Methods: For 39 consecutive patients who underwent cALND after a positive SLNB, scores were calculated using retrospective patient data for each of the three scoring systems used. Receiver operating characteristics (ROC) curves were drawn, and the areas under the curves were calculated to assess the discriminative power of each system. Univariate analysis was performed to assess the predictability of individual patient and tumor characteristics.

Results: Nonsentinel nodes were positive in 23 (59%) patients. The areas under the ROC curves were 0.63, 0.70, and 0.68, respectively. The proportion of sentinel nodes that were positive and the total number of sentinel nodes retrieved were the only individual predictors of nonsentinel node metastasis.

Conclusions: Given the high incidence of retrieving no additional metastasis on cALND, individualized patient management according to risk is desirable. Scoring systems provide additional information regarding the likelihood of metastasis in nonsentinel nodes, but their predictability remains less than optimal. The use of scoring systems must be applied with caution until future studies provide a more accurate assessment of risk for patients with a positive SLNB.

Key Words: Scoring systems • Sentinel node • Nonsentinel node • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Sentinel lymph node biopsy (SLNB) has replaced routine axillary lymph node dissection in many centers and is an accurate and reliable method of staging clinically negative axillary nodes.1–3 Whereas a negative biopsy obviates further axillary dissection and its associated morbidity,4,5 the current standard of care for a positive SLNB remains the performance of completion axillary lymph node dissection (cALND). However, metastasis to the remaining "non-sentinel" nodes on cALND is absent in 50–70% of patients with a positive SLNB, challenging the diagnostic and therapeutic benefit of categorically performing cAL-ND in all patients with a positive sentinel node.1,2,6–9 cALND has been advocated to achieve local disease control, improve survival, and aid in staging, since the histologic status of the nodes is the most powerful predictor of outcome.10–12 On the other hand, morbidity after cALND includes lymphedema, numbness, paresthesias, and motor nerve injuries, and has been reported to be mild in up to 80% of cases and moderate to severe in 18%.13,14 Therefore, accurate identification of those patients who will not derive benefit from completion adenectomy has important treatment implications.

Several studies have investigated clinicopathologic factors that may predict which patients have a higher risk of nonsentinel node involvement, none of which are sufficiently predictive when used alone.7,15–20 Scoring systems have been developed using a combination of several factors, such as tumor size, histology, hormone receptors, presence of lymphovascular invasion, the number of sentinel nodes removed, and the size of lymph node metastases as a guide to determine which patients may forego cAL-ND.6,7,15,21 The purpose of our study was to validate these scoring systems as accurate predictors of metastasis in nonsentinel lymph nodes in breast cancer patients with a positive SLNB.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Study design and population
This is a retrospective cohort study of consecutive patients with breast cancer, who underwent SLNB between January 2001 and July 2005 at Harbor-UCLA Medical Center, in Torrance, California. Harbor-UCLA is a public urban teaching hospital that serves a socioeconomically disadvantaged, racially and ethnically diverse population in southern California. Patients were included in this study if they met the following criteria: (1) a pathological diagnosis of primary invasive breast cancer; (2) a clinically negative axilla; and (3) a positive SLNB. Patients with carcinoma in situ and those who had undergone neoadjuvant chemotherapy were excluded.

Data collection
Patient data were collected from an existing Breast Diagnostic Center database as well as from individual patient medical records. This database is prospectively updated, and contains demographical information, tumor markers, the results of radiologic and pathologic tests, and a record of surgical procedures and adjuvant therapies. To ensure accuracy and completeness, the permanent medical record was reviewed for each patient.

Technique of SLNB
Sentinel lymph nodes were mapped in all cases using a subareolar injection of 500 mc of 0.22-µm filtered 99m-Tc Sulfur Colloid in a volume of 5 mL along with 5 mL of a blue dye (Methylene blue; American Regent, Inc, Shirley, NY, USA or LymphazurinTM; USSC, Norwalk, CT, USA). A handheld probe was used to determine radioactivity levels in the axilla. A sentinel node was defined as a node in the path of a blue-stained lymphatic, a blue node, or a node with counts at least tenfold those of the background. The SLNB and the histopathologic evaluation of sentinel nodes were performed in each case in accordance with a previously published protocol.22

Scoring systems
Four scoring systems were identified in the existing medical literature using a Medline-based search engine. One of the four systems was excluded from this validation study because pathological processing of sentinel nodes at our hospital does not routinely include the exact measurement of lymph node metastases larger than 2 mm.15 The first scoring system [Memorial Sloan-Kettering (MSK) score] is a nomogram from Memorial Sloan-Kettering Cancer Center that includes eight characteristics (i.e., nuclear grade, lymphovascular invasion, multifocality, estrogen receptor status, number of positive and negative sentinel nodes, tumor size, and method of detection of sentinel node metastasis) that ultimately generates a total point value, which then corresponds to a percentage of risk.21 The second scoring system [M.D. Anderson (MDA) score] was developed at the M.D. Anderson Cancer Center, and is based on four characteristics (i.e., tumor size, number of sentinel nodes, size of metastasis, and lymphovascular invasion), where a ß coefficient was determined for each, and the sum of rounded coefficients results in a score ranging from –2 to 4.6 The third system (Tenon score) was derived at the Hôpital Tenon in Paris, France, and includes three characteristics (i.e., size of metastasis, tumor size, and proportion of sentinel nodes involved) which are assigned point values that, when added, result in a score between 0 and 7.7

Data management and statistical analyses
All data were entered into an electronic spreadsheet (Microsoft Excel, Microsoft Corporation, Redmond, WA, USA) and transferred into native SAS format using translational software (dfPower DBMS/Copy; DataFlux Corporation, Cary, NC, USA). All statistical analyses were performed using either SAS Version 9.1 (SAS Institute, Inc., Cary, NC, USA) or Stata Version 8 (Stata Corporation, College Station, TX, USA).

Descriptive statistics are reported for all variables. Continuous data are reported as means with standard deviations (SD) or medians with interquartile ranges (IQR), depending on whether their distributions are normal or not, respectively. Categorical data are reported as percentages with 95% confidence intervals (95% CI). The discriminatory accuracies of the three scoring systems were compared by constructing receiver operating characteristics (ROC) curves and measuring areas under these curves (AUC). A non-parametric curve-fitting algorithm was used to construct each ROC curve because of the relatively small sample size and the likelihood that the data were non-normally distributed. Each AUC is reported with a 95% CI.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
During the 4-year period studied, 225 patients underwent SLNB at our center, 51 (23%) of which had a positive node. Three (6%) patients were excluded from the analysis due to insufficient data for the calculation of scores, leaving 48 patients. Of these, only 39 (81%) underwent cALND, and this group therefore comprised our study sample. The remaining nine patients had micrometastasis found on final pathologic processing, and did not undergo completion adenectomy.

All patients in the study were female, with a median age of 53 (IQR: 45–62) years. The median tumor diameter was 25 (IQR: 17–40) mm, and a median of 20 (IQR: 15–22) nodes were dissected during cALND. Nonsentinel nodes were positive in 23 (59%) patients. Five (13%) patients had micrometastasis to the sentinel node, defined as metastasis measuring less than 2 mm. Additional descriptive characteristics are listed in Table 1Go. Sentinel node and cALND results are listed in Table 2Go.


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  		TABLE 1. Patient and tumor characteristics
 

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  		TABLE 2. Outcomes of SLNB and cALND
 
The areas under the ROC curves were 0.63 (95% CI: 0.46–0.81), 0.70 (95% CI: 0.51–0.88), and 0.68 (95% CI: 0.51–0.85) for the MSK score, MDA score, and Tenon score, respectively (Figs. 1Go–3GoGo). The CI for the three AUC overlap, thus demonstrating no statistically significant difference between the scoring systems.


Figure 1
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  		FIG. 1. Receiver operating characteristics curve for the Memorial Sloan-Kettering nomogram.

 

Figure 2
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  		FIG. 2. Receiver operating characteristics curve for the MD Anderson scoring system.

 

Figure 3
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  		FIG. 3. Receiver operating characteristics curve for the Hôpital Tenon score.

 
When categorized into the individual factors that make up each scoring system, the only two factors that were statistically predictive were the total number of sentinel nodes and the proportion of positive sentinel nodes retrieved. Tumor size, nuclear grade, hormone receptor status, Her-2-Neu status, lymphovascular invasion, multifocality, and size of sentinel node metastasis were not statistically associated with the prediction of nonsentinel node metastases (Table 3Go). The small sample size limited any further analysis of the two significant variables and prohibited the development of a new scoring system based on this data alone.


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  		TABLE 3. Univariate analysis of tumor characteristics and the likelihood of nonsentinel node metastasis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
There is a growing body of literature to suggest that, in breast cancer patients with a clinically negative axilla and a positive SLNB, cALND may no longer be necessary in every case.19,23–25 Historically, axillary dissection has been considered important to achieve adequate staging, to decrease local recurrence, and to improve disease-specific survival.10–12 Currently, however, SLNB has been accepted as an accurate yet less invasive staging method. In addition, two large prospective clinical trials have shown that axillary radiation is equivalent to axillary dissection with respect to 10-year survival and recurrence.26,27 In a majority of cases, the remainder of nodes in the axilla on cALND after a positive SLNB show no further metastatic disease.1,2,6–9 Therefore, scoring systems have been proposed as useful tools to help identify this group of women that are at low risk of having additional nonsentinel node metastasis in the axilla.

In this study, we aimed to evaluate three previously derived scoring systems, and found that each is a fair predictor of nonsentinel node metastasis in patients with breast cancer and a positive SLNB, with areas under the ROC curves approaching 0.70. In other words, there is a 70% chance that the scoring system would predict a positive nonsentinel node in a woman with a truly positive cALND, which is better than chance (0.50), but far from perfect (1.00). Although not optimal, scoring systems have been shown to perform significantly better than the expert opinion of 17 breast cancer specialists, where predictive accuracy reached only 54%, not much better than the flip of a coin.28 Scoring systems therefore, play an important role in assessing the risk of further non-sentinel node metastasis, but must be optimized in future studies to improve accuracy.

To our knowledge, this is the first study aimed at validating both the MDA score and the Tenon score in a group of patients outside the populations in which they were developed. Conversely, the MSK nomogram has been validated twice using a prospective patient group from within Memorial Sloan-Kettering Cancer Center and once in a regional teaching hospital in the Netherlands. AUC from these studies ranged from 0.72 to 0.77.21,28,29 This appears to be substantially better than the performance of the nomogram in our population (AUC 0.63), and likely reflects substantial differences between the two study populations. Memorial Sloan-Kettering is a tertiary referral center, and the Dutch have a standardized screening program every 2 years for the general population. Our patients are predominantly nonscreened, generally younger, and represent a racially and ethnically diverse group of patients who often present with already palpable tumors and more advanced disease. This may suggest that age, racial and ethnic background, and method of cancer detection need to be considered as components of the scoring systems to make them more generalizable to all populations.

Prior to the development of scoring systems, numerous authors investigated individual tumor and sentinel node characteristics with respect to the likelihood that residual axillary nodes harbor additional metastases after a positive SLNB. Our data suggest that the proportion of positive sentinel nodes and total number of sentinel nodes retrieved for analysis are significant predictors of an increased risk of non-sentinel node metastasis. Other studies have reached similar conclusions.7,16,19,20 We also observed a non-statistically significant trend of a lower incidence of positive nonsentinel nodes in patients with micrometastases in the sentinel nodes relative to patients with macrometastases. In a majority of studies published on this topic, micrometastasis is associated with the lowest risk of nonsentinel node involvement.7,15,20 The lack of statistical significance in our group may be related to the relatively small size of our series and the fact that nine of the 14 patients with micrometastasis did not undergo cALND, leaving only five patients with metastases <2 mm in the study sample. Tumor size, tumor grade, lymphovascular invasion, and extracapsular invasion of the sentinel node have all been associated with an increased probability of nonsentinel node metastases in other studies.6,7,15,17–19 However, none of these factors were predictive in our patients. Future multi-institutional studies should be aimed at determining the exact combination of factors that should be included within a scoring system and the relative influence of each factor on the final score.

We observed positive nonsentinel nodes in 59% of our patients with a positive SLNB, higher than the 30–50% reported in the literature.1,2,6–9 There are two likely explanations for this finding. First, as mentioned earlier, micrometastasis is under-represented in our study sample. Nine patients with micrometastasis did not undergo cALND, and were therefore excluded from our final analysis. These patients accounted for 64% of those with micrometastasis in our group. Had these patients undergone cALND, the number of involved nonsentinel nodes would certainly have been lower, and may have been less than 50%. Secondly, the average tumor size in our patients is larger than that reported by others. For example, Farshid et al. reported an average tumor size of around 12 mm associated with a 46.3% rate of nonsentinel node metastasis, whereas the average tumor size in our group was approximately 29 mm.15

The introduction of SLNB has decreased the need for axillary adenectomy in nearly two-thirds of patients with a clinically negative axilla. With accurate risk stratification, over half of the remaining third, can also be spared cALND. It is becoming apparent that performing complete axillary dissection routinely on patients with a positive SLNB is not likely to positively impact outcomes and may add to morbidity. However, a clinical trial designed to answer this question has recently been closed prematurely due to slow accrual (ACOSOG Z-10011), and the issue remains to be studied. Meanwhile, we suggest that treatment of the axilla may not be significantly different from the treatment of breast cancer at the primary site. Just as a patient receives counseling about her options for breast conservation, she may now have the option for "axillary conservation" and limit morbidity resulting from an axillary dissection that is often unnecessary. Balancing a patient’s quality of life and preferences with a good oncologic outcome is then possible. Selective radiotherapy may still be an important component to achieve acceptably low recurrence rates in the axilla as it is currently used to treat residual microscopic foci of cancer in the breast, and all patients with a positive SLNB should be considered for systemic therapy. Scoring systems aid in risk stratification, thus allowing a woman and her doctor to make a decision whether or not to forego axillary dissection.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Given the high incidence of retrieving no additional metastasis on cALND, individualized patient management based on risk is desirable. Scoring systems provide additional information regarding the likelihood of metastasis in nonsentinel nodes, but predictability remains less than optimal. The three scoring systems were comparable, as determined by their AUC, but lacked sufficient predictability to be called valid. The use of scoring systems must be applied with caution until future studies provide a more accurate assessment of risk for patients with a positive SLNB.


   ACKNOWLEDGMENTS
 
The authors would like to thank Melissa Burla, MSN, NP and Katherine Gonzalez, RN for their contributions to this work.

Received for publication July 26, 2006. Accepted for publication July 27, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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