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10.1245/ASO.2005.04.020
Annals of Surgical Oncology 12:34-40 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Axillary Recurrence After Sentinel Node Biopsy

Jacqueline Sara Jeruss, MD, PhD1, David J. Winchester, MD1,2, Stephen F. Sener, MD1,2, Erika M. Brinkmann, MD1,2, Malcolm M. Bilimoria, MD1,2, Ermilo Barrera, Jr., MD1,2, Eihab Alwawi2, Angel Nickolov2, G. M. Schermerhorn2 and David J. Winchester, MD1,2

1 Feinberg School of Medicine, Northwestern University, 303 E. Chicago Avenue, Chicago, Illinois 60611
2 Evanston Northwestern Healthcare, 2650 Ridge Avenue, Evanston, Illinois 60201

Correspondence: Address correspondence and reprint requests to: David J. Winchester, MD; E-mail: djwinch{at}northwestern.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Sentinel node biopsy (SNB) has evolved as the standard of care in the surgical staging of breast cancer. This technique is accurate for surgical staging of axillary nodal disease. We hypothesized that axillary recurrence after SNB is rare and that SNB may provide regional control in patients with microscopic nodal involvement.

Methods: With institutional review board approval, SNB was performed with peritumoral injection of 99mTc-labeled sulfur colloid. From 1996 to 2003, 1167 patients were entered into a prospective cancer database after surgical therapy; 916 patients consented to long-term follow-up. Fifty-two patients (5.7%) did not map successfully and were excluded, leading to a study population of 864 patients. The median follow-up was 27.4 months (range, 1–98 months).

Results: The median number of sentinel nodes harvested was 2, and 633 (73%) patients had negative sentinel nodes. Thirty (4.7%) of those sentinel node–negative patients underwent completion axillary dissection, whereas 592 (94%) patients were followed up with observation. A total of 231 (27%) had positive sentinel nodes: 158 (68%) of these patients underwent completion axillary dissection, and 73 (32%) were managed with observation alone. Two (.32%) patients who were sentinel node negative had an axillary recurrence; one of these patients had undergone completion axillary dissection. No patient in the observed sentinel node–positive group had an axillary recurrence (odds ratio, .37; P = .725).

Conclusions: On the basis of a median follow-up of 27.4 months, axillary recurrence after SNB is extraordinarily rare regardless of nodal involvement, thus indicating that this technique provides an accurate measure of axillary disease and may impart regional control for patients with node-positive disease.

Key Words: Sentinel node biopsy • Axillary recurrence • Breast cancer • Surgical staging


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Over the last several decades, there has been a paradigm shift in surgical therapy from radical resection to increasing levels of tissue preservation. The objective of this approach has been to provide patients with optimal surgical treatment while simultaneously decreasing surgical morbidity. Breast cancer surgery has directly reflected this change in management: the standard of care for this disease has evolved from the Halstedian radical mastectomy to breast conservation for most patients. This transition has resulted from large clinical trials that have established that less radical surgery is safe and effective.1–3

A level I or II axillary dissection has been a standard of surgical care for breast cancer. This operation has been an important intervention to provide crucial staging information and regional control, but it does not seem to confer a survival benefit.1,4,5 Additionally, axillary dissection has been associated with morbid lymphedema, pain, seroma formation, poorer cosmesis, and infection.6–8 As patients have been diagnosed with earlier-stage disease, a less radical approach to the management of axillary lymph nodes has evolved.

The introduction of sentinel node biopsy (SNB) into breast cancer care marks a further progression in our understanding of this disease and has permitted a less extensive surgical option for many breast cancer patients.9–13 SNB allows the removal of fewer lymph nodes and has afforded a more targeted evaluation of the sentinel nodes, with decreased morbidity when compared with axillary dissection.6–8,14 The identification of histologically negative sentinel nodes indicates that an axillary dissection is unnecessary.7,9,12,15–17 The role of axillary dissection for patients with microscopic involvement of the sentinel nodes remains in question.

The utility of SNB in comparison with axillary dissection in clinically node-negative patients is the focus of the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-32 trial. Results from this study and the American College of Surgeons Oncology Group Z0010 and Z0011 studies will ultimately be necessary to reveal regional recurrence outcomes in a prospective randomized fashion in node-negative and node-positive patients.7,18 Thus far, 2 preliminary studies with 31 and 46 women with positive sentinel nodes and no further axillary surgery have recently been published. They showed no incidence of axillary recurrence after at least 2 years of follow-up. The extent of nonsentinel nodal involvement has been shown to decrease with smaller primary tumors and decreased axillary tumor burden. Thus, axillary dissection may have more limited utility with early-stage disease.

This study was a prospective evaluation of 864 nonrandomized clinically node-negative patients who underwent SNB and then either had completion axillary dissection or were observed. Patient and tumor prognostic factors and the incidence of axillary recurrence were examined for each group of the study population. We hypothesized that SNB provides accurate surgical staging and regional control, as reflected by a low risk of axillary recurrence.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From 1996 to 2003, under institutional review board–approved protocol EH88-077, 1167 patients were entered onto a prospective breast cancer database after surgical therapy. Of these patients, 916 consented to long-term follow-up. A total of 52 patients (5.7%) did not undergo successful lymph node mapping and were excluded, leading to a study population of 864 patients. After SNB, patients underwent axillary dissection or were managed with observation alone (Table 1Go). Outside of clinical trial participation, axillary management was determined primarily by physician and patient preference. Eleven (4.5%) sentinel node–negative patients were found to have a false-negative SNB, defined as a negative sentinel node with one or more positive nonsentinel nodes (nodes adjacent to sentinel nodes or prominent nodes seen in the dissection field). The median follow-up time was 27.4 months (range, 1–98 months).


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  		TABLE 1. Patient study populations
 
SNB Procedure
Under institutional review board–approved protocol EH97-016, SNB was performed with a four-quadrant peritumoral injection of 99mTc-labeled sulfur colloid at least 4 hours before surgery. All patients received injections of 37mBq (1mCi) 99mTc sulfur colloid diluted in an 8-mL volume. Lymphoscintigraphy was performed before surgery. If needed, a vital blue dye (isosulfan blue or methylene blue) was injected to facilitate the location of nonmapping sentinel nodes. Intraoperative localization of sentinel nodes was accomplished with a handheld gamma probe (C-Trak). If identified, internal mammary nodes were removed, according to patient and surgeon preference. Lymph nodes with ex vivo counts greater than three times the lymph node basin background level were considered sentinel nodes.12,19

Analytical Pathology
Sentinel nodes were examined through 10 serial sections at 20-µm intervals. Sections were then embedded in formalin and stained with hematoxylin and eosin. Patients with more than three sentinel nodes removed had only the three nodes with the highest counts examined with serial sections. Additional sentinel and nonsentinel nodes were examined through conventional bivalving, yielding one hematoxylin and eosin–stained slide per node.12

Treatment, Follow-Up, and Data Analysis
When appropriate, patients received adjuvant systemic therapy and radiotherapy. Radiotherapy fields were not altered to include the axilla in any patient group. Individual patient characteristics and treatment regimens were entered onto a prospective database. Study patients were assessed for nodal status, size of nodal metastasis, discovery of additional nodal involvement with axillary dissection, and incidence of axillary recurrence. Patients were examined at 6-month intervals after completion of their therapy. Follow-up information was collected and entered prospectively. Odds ratios were compared across patient groups with a {chi}2 test. A P value <.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Demographics
The mean age for the study population of 864 patients was 58 years (Table 2Go). A total of 292 (34%) patients were premenopausal, and 572 (66%) were postmenopausal. Six hundred ninety-nine (81%) patients had ductal carcinoma, 120 (14%) patients had lobular carcinoma, and 45 (5%) patients had mixed ductal/lobular pathology. Six hundred thirty-six (74%) patients underwent lumpectomy, and 228 (26%) underwent total mastectomy. The average tumor size was 1.7 cm. Forty-six (5%) patients had T0 disease; 64 (7%), T1a disease; 194 (22.5%), T1b disease; 350 (41%), T1c disease; 187 (22%), T2 disease; 19 (2%), T3 disease; and 4 (.5%), T4 disease. Nodal involvement was statistically different between T categories: 2 (4.3%) T0, 4 (6.3%) T1a, 23 (11.8%) T1b, 106 (30.3%) T1c, 90 (48%) T2, 14 (73.7%) T3, and 3 (75%) T4 (Table 2Go; P < .001). Two hundred forty-seven (32%) patients had grade 1 disease, 317 (40%) had grade 2 disease, and 220 (28%) had grade 3 disease (46 patients had T0 disease, and 34 patients did not have pathologic grade information available). Six hundred sixty-seven (77%) patients were estrogen receptor (ER) positive, and 197 (23%) patients were ER negative. Of those patients treated with lumpectomy, 546 (86%) received radiotherapy, and 90 (14%) did not. Of the patients treated with mastectomy, 41 (18%) patients received additional radiotherapy, and 187 (82%) did not. A total of 42% of patients received adjuvant chemotherapy, and 70% of patients received adjuvant antihormonal therapy (Table 2Go).


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  		TABLE 2. Patient demographics for the entire study population of 864 patients
 
Sentinel Node–Negative Patients
A total of 633 (73%) patients were sentinel node negative; 11 patients had false-negative sentinel node biopsies and were excluded from further analysis. None of the patients with a false-negative SNB has had a recurrence.

The average tumor size for the sentinel node–negative population was 1.5 cm. Remaining demographics for this patient group reflected the demographics of the entire study population (data not shown). The median number of sentinel nodes harvested was 2, and the median number of nonsentinel nodes harvested was 0. Thirty (4.7%) of the sentinel node–negative patients underwent a completion axillary dissection, with a median of 14 additional nodes harvested. One patient had an isolated axillary recurrence 24 months after her initial operation. This patient had a 2.0-cm grade 3 tumor and was initially treated with total mastectomy (nine axillary nodes removed), adjuvant chemotherapy, and hormonal therapy. Most (n = 592; 94%) of the sentinel node–negative patients were followed up with observation alone. One (.16%) patient in the sentinel node–negative observation group had an isolated axillary recurrence 22 months after her initial operation. This patient had a 4.0-cm grade 2 tumor and was initially treated with mastectomy, adjuvant chemotherapy, and hormonal therapy. Both patients with axillary recurrences remain disease free after their subsequent therapy; neither patient received chest wall or axillary radiotherapy. Overall, there was no association with recurrence in sentinel node–negative patients who underwent axillary dissection or observation of the axilla (P = .094).

Sentinel Node–Positive Patients
A total of 231 (27%) patients had sentinel node–positive disease, with an average of 1.6 involved sentinel nodes and 2.9 involved sentinel and non-sentinel nodes (Table 3Go). The average tumor size for this patient population was 2.3 cm and was distributed as follows: 6 (3%) T1a, 23 (10%) T1b, 102 (44%) T1c, 84 (36%) T2, 13 (6%) T3, and 3 (1%) T4. Of these patients, 35 (16%) had grade 1 disease, 109 (49%) had grade 2 disease, and 77 (35%) had grade 3 disease (pathologic grade information was unavailable for 10 patients).


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  		TABLE 3. Patient demographics for 231 sentinel node–positive patients
 
One hundred fifty-eight (68%) sentinel node–positive patients underwent completion axillary dissection (Table 4Go). The mean age for this patient population was 57 years, the mean tumor size was 2.4 cm, the mean and median number of sentinel nodes were 1.8 and 1, respectively, the median number of additional nodes harvested during axillary dissection was 12, and the mean follow-up was 28.6 months. Seventy-six (48%) of these patients had additional axillary disease, with an average total number of 3.7 (median, 2) positive nodes. Thus, an average of 1.9 additional positive nodes were yielded through completion axillary dissection. The median size of nodal metastasis for patients undergoing axillary dissection was 7 mm; the mean size was 8.4 mm (Table 5Go). Of the patients managed with breast-conserving surgery, 85% received radiotherapy. Eighty-one percent received systemic therapy. No sentinel node–positive patient who underwent completion axillary dissection has had an axillary recurrence.


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  		TABLE 4. Tumor and patient factors for sentinel node–positive patients managed with observation and axillary dissection
 

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  		TABLE 5. Pathologic variables for sentinel node–positive patients managed with observation and axillary dissection
 
The remaining 73 (32%) sentinel node–positive patients were managed with observation alone (Table 4Go). The mean follow-up for this patient population was 27.6 months, with a mean age of 59 years. The mean tumor size for these observed patients was 1.9 cm, the mean number of positive sentinel nodes was 1.2 (median, 1), and the median number of nonsentinel nodes harvested was 0. The median size of nodal metastasis for patients managed with observation alone was 1 mm (median, 2.7 mm; Table 5Go). Tumor size and pathologic grade distribution for this patient population was reflective of the larger sentinel node–positive patient population (Table 3Go). In this group, 58 (79%) of the observed sentinel node–positive patients were ER positive, and 15 (21%) were ER negative. Of the patients managed with breast-conserving surgery, 92% underwent radiotherapy. Eighty-five percent received adjuvant systemic therapy. No patient in the sentinel node– positive observation group has had an axillary recurrence (odds ratio, .37; P = .725). Management with axillary dissection or observation had no influence on recurrence in node-positive patients (P = .578).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Axillary recurrence is rare, regardless of sentinel lymph node status or concomitant axillary dissection, at the time of surgery. This implies that SNB provides staging information as well as regional control of clinically occult disease. In this study, the 73 patients who were observed with positive sentinel nodes had, on average, slightly larger and higher-grade tumors than the overall study population. With regard to the other examined factors (age, ER positivity, and adjuvant chemotherapy and hormonal therapy), the observed sentinel node–positive group was similar to the overall study population. No patient in the sentinel node–positive group followed up by observation or axillary dissection has experienced an axillary recurrence, whereas two sentinel node–negative patients have had an axillary recurrence.

A regional recurrence after a level I or II axillary dissection is unusual, occurring in .5% to 3% of patients.1,22,23 All patient groups in this study had a recurrence rate below that expected for patients undergoing axillary dissection. This lower-than-expected rate of axillary recurrence may reflect a lower-risk patient population and the effects of adjuvant radiotherapy, chemotherapy, and hormone therapy on residual microscopic disease.

The incidence of an axillary recurrence after negative sentinel biopsy was also significantly lower than the false-negative rate of 4.5% found in this study. This false-negative rate is consistent with reports by others.9,17,24 Disparity between the false-negative rate and the recurrence rate may reflect the duration of follow-up, the beneficial effects of radiation and systemic therapy, and the uncertain import of subclinical disease.17 When comparing the false-negative rate of the SNB with that of axillary dissection, it is not possible to define the false-negative rate of an axillary dissection as compared with the sentinel node evaluation. Giuliano et al.25 reported that overall, there is an increase in sensitivity when staging with a sentinel lymphadenectomy as compared with an axillary dissection. This improved staging with sentinel lymphadenectomy may reflect a more intensive evaluation of important nodes. If there is an increased sensitivity of sentinel lymphadenectomy over axillary dissection, this may in part explain the lower-than-expected risk of recurrence as compared with historical series of patients undergoing axillary dissection alone. However, in this report, 48% of sentinel node–positive patients were found to have additional axillary disease on completion axillary dissection. This finding is consistent with other reports that measured an incidence of 34% to 40% of additional axillary disease.19,26,27 Further follow-up of patient populations such as this one and of the NSABP B-32 and American College of Surgeons Oncology Group trials will be important to validate the accuracy of SNB and the risk of regional recurrence after sentinel lymphadenectomy alone.7,18

Of the small population of sentinel node–negative patients who underwent immediate completion axillary dissection, one patient developed an axillary recurrence 2 years after the primary treatment. This patient is exceptional in that both SNB and completion axillary dissection failed to detect and contain nodal disease at the time of the initial surgery. Axillary recurrence after axillary dissection is uncommon and has been attributed to anatomical variation in the distribution of axillary nodal tissue.22 The advent of SNB has generated concern regarding the potential for undertreatment and understaging of axillary disease, because axillary recurrence occurring within 2 years of axillary dissection has been associated with poor prognosis.22 One patient in the observed sentinel node–negative group in this study has had an axillary recurrence. According to review of a compilation of published reports, the overall rate of axillary recurrence for 2271 sentinel node-negative patients was .4% (Table 6Go).16


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  		TABLE 6. Case series and case reports of recurrence after negative SNB
 
The median number of nonsentinel nodes for each group of observed patients was 0. In a study of 415 breast cancer patients undergoing concurrent axillary dissection, a five-node biopsy provided a 97.3% sensitivity to identify lymph node metastases found in the entire axillary dissection.28 However, Mathiesen et al.29 found that the rate of node positivity in- creased incrementally until 10 nodes were removed from the axilla. Added together, the number of nonsentinel nodes and sentinel nodes for each group did not approach either of these thresholds, thus suggesting that aggressive removal of nonsentinel or sentinel nodes did not contribute significantly to the local control of these diseases.

In the NSABP B-04 trial, 18.6% of clinically node-negative patients who were managed with total mastectomy and axillary observation developed palpable disease that required axillary dissection.1 This indicates that in a patient population not receiving any adjuvant radiation or systemic therapy, fewer than half of the patients with microscopic nodal involvement develop clinical manifestations of their axillary disease.1 Neoadjuvant chemotherapy has been associated with a decrease in the incidence of axillary node positivity, as shown by the NSABP B-18 trial.30 Currently most patients with tumors >1 cm receive some form of systemic therapy. Eighty-five percent of the observed sentinel node–positive patients in this study received adjuvant systemic therapy. After >2 years of follow-up, no patient in the observed sentinel node–positive group has sustained an axillary recurrence. This outcome is consistent with the findings of Fant et al.19 and Guenther et al.,20 who studied smaller node-positive study populations. In this study, the patients observed in the sentinel node–positive group had fewer involved sentinel nodes and smaller nodal micrometastases than the patients in the axillary dissection group. A smaller burden of residual microscopic axillary disease, along with the use of adjuvant therapy, may, in combination, account for the low rate of axillary recurrence in this study.

The significance of a complete axillary dissection to define systemic therapy has been called into question. A recent study of risk stratification based on patient age and sex, tumor size, hormone receptor status, nuclear grade, and the presence of lymphovascular invasion demonstrated that knowledge of nodal status was not imperative to the decision to administer adjuvant chemotherapy.31 Therefore, as more patients are diagnosed with early-stage disease localized to the breast and as treatment plans are more routinely made on the basis of tumor factors, a complete analysis of the axilla becomes less critical. The argument for axillary dissection remains for patients with palpable disease who stand to benefit from a therapeutic node dissection.

Breast cancers are evaluated most consistently by stage and pathologic grade. The accuracy of stage and grade is not precise, and this results in subsets of patients who are undertreated and overtreated. Consequently, new methods for evaluating breast cancer are necessary to bring crucial refinement to disease prognosis and treatment. The development of SNB for breast cancer has helped to facilitate this refinement, and clinical trials, such as the Z0011 study, will aid in determining the ultimate utility of this technique as a means for establishing definitive breast cancer prognosis and regional control. This preliminary work supports the diagnostic utility of SNB and the role of observation in both sentinel node–negative and positive early-stage breast cancer patients.


   ACKNOWLEDGMENTS
 
We thank Mary Turk and Dr. Stacey C. Tobin for their assistance in preparing this manuscript.

Received for publication April 12, 2004. Accepted for publication September 20, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Micrometastases in Sentinel Lymph Node in a Multicentric Study: Predictive Factors of Nonsentinel Lymph Node Involvement--Groupe Des Chirurgiens De La Federation Des Centres De Lutte Contre Le Cancer
J. Clin. Oncol., April 20, 2006; 24(12): 1814 - 1822.
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L. A. Newman
Lymphatic Mapping and Sentinel Lymph Node Biopsy for Breast Cancer Patients
J. Oncol. Pract, November 1, 2005; 1(4): 130 - 133.
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