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Annals of Surgical Oncology 10:126-130 (2003)
© 2003 Society of Surgical Oncology

ORIGINAL ARTICLES

Preliminary Outcome Analysis in Patients With Breast Cancer and a Positive Sentinel Lymph Node Who Declined Axillary Dissection

Jerri S. Fant, MD, Michael D. Grant, MD, Sally M. Knox, MD, Sheryl A. Livingston, MSN, RN, Kimberly Ridl, MD, Ronald C. Jones, MD and Joseph A. Kuhn, MD

From the Department of Surgery, Baylor University Medical Center, Dallas, Texas.

Correspondence: Address correspondence and reprint requests to: Joseph Kuhn, MD, 3409 Worth Street, Suite 420, Dallas, TX 75246; Fax: 214-824-7167; E-mail: kuhndallas{at}aol.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: This retrospective study was designed to provide a preliminary outcome analysis in patients with positive sentinel nodes who declined axillary dissection.

Methods: A review was conducted of patients who underwent lumpectomy and sentinel lymph node excision for invasive disease between January 1998 and July 2000. Those who were found to have sentinel lymph node metastasis without completion axillary dissection were selected for evaluation. Follow-up included physical examination and mammography.

Results: Thirty-one patients were identified who met inclusion criteria. Primary invasive cell types included infiltrating ductal carcinoma, infiltrating lobular carcinoma, and mixed cellularity. Most primary tumors were T1. Nodal metastases were identified by hematoxylin and eosin stain and immunohistochemistry. Twenty-seven of the metastases were microscopic (<2 mm), and the remaining four were macroscopic. All patients received adjuvant systemic therapy. With a mean follow-up of 30 months, there have been no patients with axillary recurrence on physical examination or mammographic evaluation.

Conclusions: We have presented patients with sentinel lymph nodes involved by cancer who did not undergo further axillary resection and remain free of disease at least 1 year later. This preliminary analysis supports the inclusion of patients with subclinical axillary disease in trials that randomize to observation alone.

Key Words: Sentinel lymph node • Micrometastasis • Completion axillary dissection • Axillary recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Sentinel lymph node (SLN) biopsy has become a popular alternative to level I and II axillary dissection for staging in patients with invasive breast cancer because of the improvement in microscopic staging and a decrease in the incidence of lymphedema.1,2 Early validation studies of this technique required a SLN biopsy followed by a complete axillary dissection.3 As experience evolved, many institutions began to offer SLN biopsy without simultaneous axillary dissection.4 When the SLN was found to have metastatic involvement, the standard of care was to proceed with completion axillary dissection. However, the likelihood of finding additional positive nodes is relatively small in patients with micrometastasis.5,6 In some cases, patients choose to avoid complete dissection to eliminate the potential risk of lymphedema or nerve injury.7,8 A prospective, national trial (American College of Surgeons Oncology Group [ACOSOG] Z0011) is under way to determine whether further surgery to remove level I and II nodes is necessary. Patient accrual may be hindered by a lack of data regarding the safety of removing only the SLNs. This retrospective study was designed to provide a preliminary outcome analysis in patients with positive sentinel nodes who did not undergo subsequent axillary dissection.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
A retrospective, institutional review board-approved chart review was conducted on patients who underwent SLN biopsy and lumpectomy for invasive breast cancer over 3 years. All patients who were found to have a positive SLN by routine histology or cytokeratin staining and who declined completion dissection were included in the study. Retrospective analysis was conducted of patient demographics, tumor characteristics, adjuvant therapy, and subsequent clinical course. Recent mammography and physical examination findings were reviewed to determine the incidence of axillary recurrence.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Approximately 360 patients underwent SLN biopsy and lumpectomy for invasive breast cancer at Baylor University Medical Center between January 1998 and June 2000. Lymph node metastasis was identified in 102 patients. Thirty-one of these patients declined the recommended completion axillary dissection (30%). Invasive tumor cell types included infiltrating ductal carcinoma (n = 25), infiltrating lobular carcinoma (n = 4), and mixed cellularity (n = 2). Most primary tumors were T1 (n = 25) and ranged in size from .3 to 1.8 cm. There were six T2 primary tumors that ranged in size from 2.2 to 3.2 cm (Table 1). Focal, peritumoral lymphovascular invasion was identified in six cases. Seventeen primary tumors were located in the upper outer breast quadrant, whereas the remaining 14 tumors were more equally distributed between the other 3 quadrants and central locations (Fig. 1). Nodal metastasis was identified by hematoxylin and eosin stain (n = 20) and immunohistochemistry (n = 11). Twenty-seven of the metastases were microscopic (<2 mm), and the remaining four were macroscopic. The total number of sentinel nodes identified and the total positive nodes in each patient varied (Table 2). Twenty patients (64%) had only one positive SLN. Immunohistochemistry was routinely performed on all sentinel nodes. Standard radiotherapy (breast/chest-wall radiation with a scar boost) was completed in each case. Axillary field radiation was performed in one case. All patients received adjuvant systemic chemotherapy. Twenty-six patients had estrogen receptor-positive tumors and received hormonal therapy (tamoxifen or anastrozole).


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  		TABLE 1. Tumor characteristics
 


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  		FIG. 1. Tumor location. UOQ, upper outer quadrant; UIQ, upper inner quadrant; LOQ, lower outer quadrant; LIQ, lower inner quadrant.

 

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  		TABLE 2. Patient characteristics
 
With a mean follow-up of 30 months (range, 21–48 months), there have been two deaths. One woman died as a result of intracranial hemorrhage unrelated to breast cancer 16 months after lumpectomy and SLN biopsy. She was free of disease at 12-month follow-up. The second death occurred from systemic metastases identified after eight adjuvant chemotherapy cycles and standard radiotherapy. This patient originally presented with a high-grade tumor measuring 1.3 cm; one of two SLNs had a <2-mm micrometastasis. There was no clinical disease in the axilla. Preoperative abdominal computed tomography, chest x-ray, and bone scan were negative for metastatic disease. She had an additional follow-up abdominal computed tomography scan 11 months after diagnosis that was also negative. She presented 13 months after diagnosis with metastatic disease to her liver, abdomen, and bony structures of the spine and pelvis.

The remaining 29 patients had routine examinations and mammography at 6-month intervals after lumpectomy and adjuvant therapy. None of these patients has developed local recurrence or metastatic disease. There has been no evidence of axillary recurrence in this group at a mean 30-month follow-up (range, 22–51 months).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The ACOSOG Z0011 trial is a prospective study that randomizes patients with a positive SLN biopsy to either completion axillary dissection or no further surgery. Because enrollment requires blinded patient assignment, surgeon and patient bias toward complete axillary dissection as a standard of care may hinder participation. There is a paucity of data that specifically suggest equivalent patient outcome after SLN removal without completion dissection. The arguments that suggest that it may be appropriate to avoid completion dissection fall into the following categories: (1) the incidence of positive nonsentinel nodes is low for micrometastasis, (2) the adjuvant chemotherapy is likely to destroy any microscopic involvement, (3) information obtained from completion axillary dissection rarely alters treatment recommendations, and (4) there is no conclusive evidence that immediate dissection is better than observation and delayed dissection if metastatic growth in the axilla is subsequently noted.

This series presents a high proportion of women who refused axillary dissection. The complete discussion of treatment options for a patient who has been diagnosed with a metastatic focus in a sentinel node is complex. During the process of informed consent, it is necessary to discuss the nature of the current controversy and alternatives. Most of the eligible patients in this series were offered randomization in the Z0011 protocol; therefore, the concept of no further surgery was introduced as a potential option under investigation. Because the surgeon presents the rationale for the Z0011 protocol to a patient for consideration, the patient would have to deduce that both arms (dissection vs. no dissection) are potentially reasonable options. The limitation is the lack of comparative prospective data to present one as being equivalent or superior to the other. However, this is the same dilemma with the SLN procedure itself, because it is a procedure that is subject to validation by ongoing investigation. The outcome of such a discussion in some cases yielded the option of no further surgery for many patients in this series. This treatment course was provided with the clear explanation that prospective data are not available to answer the question of the necessity of additional surgery (especially with micrometastasis) and that an increased risk of disease spread is theoretically possible.

Several studies with SLN biopsy followed by immediate axillary dissection have shown a low incidence of residual disease. Wong et al.9 found further axillary disease in 144 (37%) of 389 patients with a positive sentinel node out of 1415 patients enrolled from multiple institutions. In a study from The Netherlands, 34% of patients evidenced residual axillary disease.10 Similarly, Abdessalam et al.11 identified only 40 of 100 patients to have additional metastasis in nonsentinel nodes. Although the size of the primary tumor, the extent of sentinel node metastasis, and the pathology technique varied, each of these studies supports a <50% risk of residual axillary disease when a sentinel node is positive. If micrometastasis alone is evaluated, the risk is lower. Ganaraj11a reported an analysis of nonsentinel nodes by serial sectioning of all nodes. There was a low incidence of positive nonsentinel nodes in patients with micrometastasis (ductal, 0%; lobular, 31%) compared with macrometastasis (ductal, 29%; lobular, 75%). Likewise, Chu et al.12 reported a 7% rate of further disease in the axilla when the SLN had a <2-mm focus of tumor and 55% if a >2-mm focus of tumor was identified. Kamath et al.,13 in evaluating SLN micrometastasis alone, found a 15% risk of residual disease.

Next, adjuvant chemotherapy may contribute to the locoregional control of axillary metastases. Furukawa et al.14 evaluated the response of lymph node metastasis to various chemotherapeutic agents and found that nodal tumor was chemosensitive. It has also been shown that patients with a primary tumor response to neoadjuvant chemotherapy are less likely to have nodal metastasis at surgery.15,16 Fisher et al.,17 in reviewing data from National Surgical Adjuvant Breast and Bowel Project B-18, found 36% of clinically node-positive patients were pathologically node negative after receiving neoadjuvant chemotherapy. Together, these studies suggest that chemotherapy is likely to ablate residual microscopic axillary metastases.

Also, information obtained from completion axillary dissection may not change the patient’s treatment. Baxter et al.18 have shown that most patients with invasive breast cancer undergo adjuvant systemic therapy regardless of axillary node status, a finding supported by the data of Fisher et al.19 and discussed by Singletary20 in her review of systemic treatment after SLN biopsy. Miltenburg et al.,21 in their meta-analysis of SLN biopsy in breast cancer, question the therapeutic benefit of total level I and II lymph node removal, estimating that 70 of 100 axillas will not contain cancer.

Finally, no data confirm an overall survival benefit with regional lymphadenectomy. The National Surgical Adjuvant Breast and Bowel Project B-04, for example, revealed no statistical difference in survival among patients undergoing radical mastectomy versus total mastectomy versus total mastectomy with radiotherapy.22 Clinicians have used these data to suggest that immediate dissection may be equivalent to observation and delayed dissection if subsequent nodes become palpable. Numerous randomized trials both confirm and disprove the necessity of surgical node removal in promoting overall survival.23–26 Orr,27 for example, analyzed six randomized trials comparing tumor resection with and without axillary lymph node dissection and found a statistically significant survival benefit with axillary lymph node dissection in only three of the six studies. It is difficult, however, to interpret this finding, because the trials included in the study were performed at least 15 years ago, and neither the surgical technique nor the adjuvant therapy was equivalent. Bland et al.28 reviewed >500,000 National Cancer Data Base patients and concluded that the omission of axillary lymph node dissection worsened survival. However, the percentages reported indicate overall survival without mention of cause of death or stratification based on year, surgical technique, or adjuvant therapy, and statistical assessment was not used. Hayward and Caleffi,29 in espousing mastectomy over breast conservation in some patients to achieve local control, admit that an increase in local recurrence is not synonymous with decreased survival. Although it is a controversial issue, evidence that level I and II axillary dissection confers a survival benefit to breast cancer patients who receive treatment after the current standard of care is conflicting and, therefore, inconclusive.

This series has presented 31 patients with disease in at least 1 SLN who did not undergo further node resection. Although nodal disease varies from micrometastasis (n = 27) to macrometastasis (n = 4), there were no clinical or radiographical recurrences in this group at a mean 30-month follow-up. Clearly, longer follow-up will be appropriate.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Limited information is available regarding the outcome of patients with positive sentinel node resection and observation after adjuvant therapy. The data presented in this study suggest that SLN biopsy without axillary dissection may be an acceptable alternative to completion axillary dissection. However, longer follow-up and prospective randomized studies are needed to delineate appropriate criteria for patient selection and confirm the safety of this approach. Patients should be encouraged to enroll in ACOSOG Z0011, which randomizes to completion dissection or no further surgery. On the basis of the preliminary results of this study, the latter approach is both ethical and justifiable.


   Footnotes
 
This retrospective study presents 31 patients with at least 1 positive sentinel lymph node who did not undergo further node resection. Although nodal disease varied from micrometastasis (n = 27) to macrometastasis (n = 4), there were no clinical or radiographical recurrences in this group at a mean 30-month follow-up.

Received for publication April 15, 2002. Accepted for publication September 23, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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