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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:145-149 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Lymphovascular Invasion Enhances the Prediction of Non-Sentinel Node Metastases in Breast Cancer Patients With Positive Sentinel Nodes

Martin R. Weiser, MD, Leslie L. Montgomery, MD, Lee K. Tan, MD, Barbara Susnik, MD, Denis Y. H. Leung, PhD, Patrick I. Borgen, MD and Hiram S. Cody III, MD

From The Breast Service, Department of Surgery (MRW, LLM, PIB, HSC), the Department of Pathology (LKT, BS), and the Department of Biostatistics (DYHL), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Dr. Hiram S. Cody III, The Breast Service, Dept. of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 212-794-5812; E-mail: codyh{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: Fifty percent of patients with sentinel lymph node (SLN) metastases have no metastatic disease in non-SLNs on axillary lymph node dissection (ALND). The goal of this study is to determine which patients have metastatic disease limited to the SLN, and, therefore, may not require completion ALND.

Methods: Of the first 1000 patients undergoing SLN biopsy at Memorial Sloan-Kettering Cancer Center, using a combined blue dye and isotope technique, 231 (26%) had positive SLN. Of these, 206 underwent completion ALND. They are the study group for this report.

Results: The likelihood of non-SLN metastasis was inversely related to three clinicopathologic variables: tumor size <= 1.0 cm; absence of lymphovascular invasion (LVI); and SLN micrometastases (<= 2 mm). None of 24 patients with all three predictive factors had non-SLN metastases, whereas 58% of patients with none of the factors had disease in the non-SLN.

Conclusion: Patients with small breast cancers, no LVI, and SLN micrometastases have a low risk of non-SLN metastases, and may not require completion ALND.

Key Words: Breast cancer • Lymph node metastasis • Sentinel node


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Sentinel lymph node (SLN) biopsy is rapidly changing the treatment algorithm for patients with breast cancer. This minimally invasive technique allows identification and biopsy of the first draining lymph nodes from the axilla, and (based on 32 published series validated by a backup axillary dissection)1–32 accurately predicts the status of the axilla in 97% of cases (Table 1). While patients with negative SLN can be spared the morbidity of a full axillary dissection (ALND),33 the treatment of patients with positive SLN is less clear. Completion ALND in this group yields additional disease in 52% of cases (range, 22–67%; Table 1). The goal of this study is to identify the histopathologic features of SLN-positive cancers that allow the prediction of non-SLN metastases, and to identify a subgroup who may not require completion ALND.


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  		TABLE 1. Results of SLN biopsy with backup ALNDa
 

   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Between September 1, 1996 and January 31, 1999, 1000 patients had SLN biopsy for clinical stage T1-2N0 breast cancer at Memorial Sloan-Kettering Cancer Center. Of 231 patients who had successful SLN mapping and positive SLN (26%), 206 had completion ALND and make up the study group for this report.

Our technique of SLN mapping used both blue dye and radioisotope in all patients, and has been described in detail previously.27,34 Successful mapping by blue dye required the identification of a blue-stained SLN or a blue-stained lymphatic directly contiguous with a non-blue node. Successful isotope mapping required the ex vivo counts of the SLN to exceed the postexcision axillary background by a factor of at least 4.

Whenever possible (depending on node size), half of each SLN was immediately frozen and banked for research protocols. A portion of the remaining nodal tissue was taken for frozen section, and examined by a single hematoxylin and eosin (H&E)-stained section. The remaining frozen tissue (submitted as a "frozen section control") and all remaining unfrozen nodal tissue was fixed and embedded in paraffin. Serial sections were taken at 50-µm intervals and stained with both H&E and immunohistochemical (IHC) stains for CAM5.2 and AE1:AE3 (Becton Dickinson Immunocytometry Systems, San Jose, CA). An average of three H&E- and two IHC-stained sections were analyzed per SLN. Non-SLN were analyzed with a single H&E-stained section.

Clinicopathologic characteristics were entered prospectively into a database and included patient age, primary tumor size, tumor location, histologic/nuclear grade, presence of lymphovascular invasion (LVI), and size of the metastatic deposit in the SLN. Based on a complete pathologic review of all SLN-positive cases, SLN deposits up to 2 mm (and including SLN that were positive only on IHC) were classified as micrometastases, and those larger than 2 mm were classified as macrometastases. Primary tumor size was dichotomized as 1 cm or less (T1a/b) vs. greater than 1 cm (T1c/T2) for the multivariate analysis.

Clinicopathologic factors associated with non-SLN metastases were assessed by {chi}2 or Fischer’s exact test when appropriate. Multivariate analysis used stepwise logistic regression.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
The median age of the 206 patients who underwent completion ALND was 52 years (range, 21–85). The median tumor size was 1.5 cm (range, 0.1–4.5 cm). One hundred eighty-one patients (88%) had infiltrating ductal carcinoma, 20 (10%) had infiltrating lobular carcinoma, and the remaining 4 (2%) had colloid, medullary, or tubular carcinoma. Of the 206 patients who underwent completion ALND, 66 (32%) had metastases in the non-SLN, with a median of 1.5 and a mean of 3.6 (range, 1–30) non-SLN involved with metastatic tumor.

On univariate analysis, clinicopathologic features associated with non-SLN metastases included primary tumor size, SLN metastasis size, and LVI by the tumor (Table 2). On multivariate analysis, only primary tumor size and SLN metastasis size were independent predictors of non-SLN metastases. The presence of LVI was not an independent predictor of non-SLN metastases, because it was highly correlated with the size of the primary tumor; 22% of patients with T1a/b tumors had LVI, vs. 45% with T1c/T2 tumors (Table 3, P = .003). Within the group of patients with smaller (T1a/b) tumors, LVI significantly predicted non-SLN metastasis (Table 3).


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  		TABLE 2. Clinicopathologic features associated with non-SLN metastases
 

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  		TABLE 3. Lymphovascular invasion predicts non-SLN metastases in small breast tumors Tumor
 
The three factors associated with SLN-only metastasis were T1a/b tumor size, absence of LVI, and micrometastatic disease in the SLN. While none of these factors by itself was sufficient to predict non-SLN metastasis, none of 24 patients with all three had disease in the non-SLN (Table 4, P < .001).


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  		TABLE 4. Primary tumor size, LVI, and SLN metastasis size predict non-SLN metastasis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
Sentinel lymph node biopsy has changed the approach to patients with operable breast cancer. By limiting the axillary exploration to those nodes most likely to contain disease, the pathologic analysis of those nodes can be intensified. Serial sectioning and IHC staining of the SLN upstage 10% to 15% of patients whose nodes are negative by conventional single-section H&E analysis.35 Conversely, if no metastases are found after thorough SLN analysis, then the chance of non-SLN metastases is exceedingly small,33 and completion ALND is unnecessary. About half of all patients with positive SLN have no residual disease in the axilla (Table 1), and would not be expected to benefit from a completion ALND. The goal of this study is to determine whether this subset of SLN-positive patients could be identified in advance, and consequently spared ALND.

By univariate analysis, smaller tumor size, SLN micrometastasis, and absence of LVI all predicted non-SLN metastases. Other studies have reported comparable results. Disease limited to the SLN was found by Chu et al.36 in 66% and by Reynolds et al.37 in 47% of SLN-positive patients. Both studies find a significant association between non-SLN metastases and (1) larger tumor size and (2) SLN macrometastases. Both also note an association between non-SLN metastasis and LVI, but not at the level of statistical significance. This may simply represent type II statistical error on the basis of small sample size, because the two studies comprise only 157 and 60 cases, respectively. Of note, a follow-up study by Chu et al.38 found a significant association between LVI and non-SLN disease when IHC was added to the pathologic analysis of the non-SLN. All of these findings are quite consistent with the observation that peritumoral LVI is a predictor of both lymph node metastasis and distant relapse.

In our analysis, no single variable predicted non-SLN metastases with sufficient accuracy that ALND could safely be omitted. Although disease in the non-SLN was significantly less likely for smaller tumors, 8% of patients with T1a and 21% of patients with T1b tumors had non-SLN metastases. Similarly, 18% of patients with SLN micrometastases and 26% of patients without LVI had non-SLN disease.

Others have combined two variables, size of tumor and size of SLN metastasis, in an effort to increase the accuracy of prediction. Reynolds et al.37 found no non-SLN disease in 18 patients with T1 tumors (<= 2 cm in diameter) and SLN micrometastases, and Chu et al.38 found non-SLN disease in none of 14 patients with T1a/b tumors (<= 1 cm in diameter) and SLN micrometastases. Both studies are limited by small sample size. In the present series, among 29 patients with T1ab tumors and SLN micrometastases, 2 patients (7%) had non-SLN metastases. Using two of the three favorable predictive variables in our own model, 26% of patients still had non-SLN metastases (Table 4).

Although not found to be an independent predictor of non-SLN metastases (because of its correlation with tumor size), LVI significantly enhanced the prediction of non-SLN metastases in patients with smaller tumors (Table 3). The most accurate prediction of non-SLN metastasis arose from the combination of the three variables that proved significant in univariate analysis: tumor size, LVI, and size of SLN metastasis. None of 24 patients with all three predictive variables (tumor <= 1.0 cm, SLN micrometastasis, and no LVI) had residual disease in the non-SLN, whereas only 43% of 40 patients with none of the three had disease limited to the SLN (Table 4).

A potential weakness in this analysis is that enhanced pathologic analysis (with serial sections and IHC staining) was used only for the SLN, whereas the non-SLN were examined routinely (with a single H&E-stained section), potentially missing non-SLN metastases. Chu et al.38 address this issue. In 157 completion ALND specimens from SLN-positive patients, the addition of IHC to routine H&E increased the detection of non-SLN metastases from 35% to 45%. For patients with T1a/b tumors, non-SLN metastases increased from 10% to 20%. However, the analysis of non-SLN by IHC is costly and labor-intensive, and adds little to the management of a patient already found to be node-positive. It remains unclear from the study of Chu et al.,38 a univariate analysis, whether prediction of non-SLN disease by a combination of histopathologic features might have achieved the same result.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
Patients with SLN metastases have a graded risk of non-SLN metastases. The proportion of patients who have metastases limited to the SLN can be predicted by combining tumor size <= 1.0 cm, the absence of LVI, and micrometastatic disease in the SLN. None of the 24 patients with all three predictive factors had non-SLN metastases, and this subset of patients may not require a completion ALND. As a cautionary note, a substantial experience was required to generate this very small subset of patients, who represent only 2.4% of our 1000 SLN biopsy procedures. Pending further clinical experience and the results of randomized trials, we feel that completion ALND remains the standard of care for most patients with positive SLN.


   Acknowledgments
 
The authors are grateful to the Tow Foundation for philanthropic grants supporting the sentinel node programs at Memorial Sloan-Kettering Cancer Center.


   Footnotes
 
Presented at the 53rd Annual Meeting of the Society of Surgical Oncology, New Orleans, Louisiana, March 16-19, 2000.

Received for publication March 17, 2000. Accepted for publication September 13, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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K. J. Van Zee, D.-M. E. Manasseh, J. L. B. Bevilacqua, S. K. Boolbol, J. V. Fey, L. K. Tan, P. I. Borgen, H. S. Cody III, and M. W. Kattan
A Nomogram for Predicting the Likelihood of Additional Nodal Metastases in Breast Cancer Patients With a Positive Sentinel Node Biopsy
Ann. Surg. Oncol., December 1, 2003; 10(10): 1140 - 1151.
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 JNMHome page
I. Brenot-Rossi, G. Houvenaeghel, J. Jacquemier, V.-J. Bardou, M. Martino, N. Hassan-Sebbag, and J. Pasquier
Nonvisualization of Axillary Sentinel Node During Lymphoscintigraphy: Is There a Pathologic Significance in Breast Cancer?
J. Nucl. Med., August 1, 2003; 44(8): 1232 - 1237.
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R. F. Hwang, S. Krishnamurthy, K. K. Hunt, N. Mirza, F. C. Ames, B. Feig, H. M. Kuerer, S. E. Singletary, G. Babiera, F. Meric, et al.
Clinicopathologic Factors Predicting Involvement of Nonsentinel Axillary Nodes in Women With Breast Cancer
Ann. Surg. Oncol., April 1, 2003; 10(3): 248 - 254.
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G Cserni
Complete sectioning of axillary sentinel nodes in patients with breast cancer. Analysis of two different step sectioning and immunohistochemistry protocols in 246 patients
J. Clin. Pathol., December 1, 2002; 55(12): 926 - 931.
[Abstract] [Full Text] [PDF]

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