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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2003.01.017 on October 13, 2003

Annals of Surgical Oncology 10:1054-1058 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Outcomes After Localized Axillary Node Recurrence in Breast Cancer

F.C. Wright, MD, FRCSC, J. Walker, MD, FRCSC, C.H.L. Law, MD, MPH, FRCSC and D.R. McCready, MD, MSc, FRCSC, FACS

From the Department of Surgery, University of Toronto, Toronto, Ontario, Canada.

Correspondence: Address correspondence and reprint requests to: D. R. McCready, MD, MSc, Department of Surgical Oncology, Princess Margaret Hospital, University of Toronto, 3-130, 610 University Avenue, Toronto, Ontario, Canada M5G 2M9; Fax: 416-946-6590; E-mail: David.McCready{at}uhn.on.ca


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Localized axillary recurrence (LAR) is an uncommon event. It is estimated to occur in 0.5% to 3% of patients when adequate axillary surgery has been performed. Although relatively sparse data exist on the outcome of patients with LAR, in the era of sentinel node biopsy (SNB) these data may have increased relevance. This study assesses the survival outcomes in these patients.

Methods: A retrospective chart review was completed. Patient age, tumor size, pathology, receptor status, and treatment of the primary breast carcinoma were reviewed. Axillary recurrence, treatment, and overall survival data were collected.

Results: Fifteen patients were identified with LAR that developed at a median of 77 months after their initial dissection. At the time of treatment for their LAR, all patients had completion axillary clearance and six also had a concurrent completion mastectomy. Further adjuvant treatment was individualized. Five patients (33%) have died, including all patients (3) who developed a LAR within 2 years of their initial breast cancer presentation. Ten-year overall survival is 56%.

Conclusion: Our experience suggests early (<24 months) LAR is indicative of a poor prognosis. With multimodal treatment, ten-year overall survival is 56%.

Key Words: Breast cancer • Axillary recurrence • Survival • Surgery


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Localized axillary recurrence (LAR) is rare. It occurs in 0.5% to 3% of all women with breast cancer after adequate axillary surgery (level I, II) has been performed. LAR is an independent predictor of distant metastases1,2 and has an associated 5-year overall survival of 35% to 49%.3,4 We predict that in the upcoming era of sentinel node biopsy (SNB), LAR will likely increase. The reported false-negative rate from multi-institutional studies with significant experience with the SNB technique is between 5% to 15%.5–8 That is, when nodal metastases are present in the axilla, the SNB misses 5% to 15% of the metastases. In addition, it is suggested that a surgeon acquiring the new skill of SNB node biopsy perform 20 to 30 SNB with a standard axillary dissection and have a detection rate of >90% and a false-negative rate of <5%.9 In practice, however, 28% of surgeons perform fewer than 10 SNB with subsequent axillary lymph node dissection before performing SNB alone.10 Thus, even if adjuvant systemic treatment and radiation reduce the chance of local disease progression, the incidence of LAR is likely to be greater after SNB compared with a level I, II axillary dissection. Knowledge of treatment, survival outcomes, and prognosis for patients who develop LAR will continue to be relevant to current practice.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patients
A retrospective chart review was completed of a single surgeon’s experience (1992–2001) with patients who presented to a tertiary care center with localized axillary recurrence at some time after a level I, II axillary dissection as part of their primary breast cancer management. Patients with distant metastases, chest-wall, or supraclavicular lymph node recurrence were excluded. Data were extracted, including patient demographics, primary breast tumor characteristics, treatment of the primary breast carcinoma, presentation, staging and treatment of the axillary recurrence, follow-up, and survival.

Statistics
Descriptive statistics were completed. A Kaplan-Meier survival curve was calculated. SPSS version 10 was used for calculations.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Fifteen female patients were identified with localized axillary recurrence after previous axillary surgery. All of these patients had disease amenable to surgery and accepted surgery as part of their multimodal treatment for this regional recurrence.

Patient Characteristics
The mean patient age at the time of the original breast cancer was 45 years (range, 30–64 years). At time of localized axillary recurrence, mean patient age was 54 years (range, 30–79 years). Median time to LAR after primary breast carcinoma was 77 months (range, 10–353 months). Three patients developed LAR within 2 years of the primary diagnosis of breast cancer. None of the 15 patients had a brief history of breast carcinoma. One patient had two first-degree relatives with breast cancer; another patient had a second-degree relative with breast carcinoma. One patient had received hormone replacement therapy for 5 years before a diagnosis of the primary breast carcinoma.

Primary Breast Cancer Characteristics
The mean size of the primary breast carcinoma was 2 cm. Of the carcinomas, 87% were invasive ductal carcinomas, 53% were estrogen receptor positive, and 60% of tumors were progesterone receptor positive. The first axillary dissection yielded a mean of eight lymph nodes in the specimen (range, 2–14). Of the 15 patients, 8 had metastatic disease in their axillary lymph nodes (range, 1–9 nodes involved with carcinoma), whereas 7 patients were considered node negative after their original axillary dissection (Table 1).


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  		TABLE 1. Primary breast cancer characteristics and treatment
 
Treatment of the Primary Breast Carcinoma
All patients had surgery for their primary breast carcinoma. Nine of the 15 patients had a lumpectomy and axillary lymph node dissection. Six had a modified radical mastectomy. Six patients who were treated with a lumpectomy and axillary lymph node dissection received radiation to the breast. None of the patients who had a modified radical mastectomy received any radiation. Six of the eight patients who were found to have lymph node metastases received chemotherapy (one refused, one patient 64 years of age was offered tamoxifen instead). Four patients received hormonal therapy, three of whom had estrogen and progesterone sensitive tumors (Table 1).

Patient Presentation with Localized Axillary Recurrence and Staging
All patients were referred to a single surgeon at a tertiary care center with a diagnosis of LAR. All axillary recurrences were detected as palpable masses on clinical examination of the axilla. None of the LAR was discovered incidentally on follow-up imaging. Patients were evaluated for metastatic spread by conventional means: physical examination, bone scan, abdominal ultrasound, and chest x-ray study. Recently, magnetic resonance imaging (MRI) has been used to assess involvement of the brachial plexus, axillary vein, and artery, which, if involved, would exclude patients from the "localized axillary recurrence" designation. The use of MRI, however, has not changed the intent of the operative procedure in any cases included in this report. Axillary recurrence was confirmed pathologically by free-hand fine needle aspiration in the clinic for all patients preoperatively.

Treatment of Localized Axillary Recurrence
Treatment was multimodal and individualized. All patients had recurrent axillary nodal metastases excised with a completion axillary dissection and six also had a concurrent completion mastectomy. At least two patients of this falsely "node-negative" group had their nodal recurrence (residual disease) under an undissected axillary arch adjacent to the latissimus dorsi muscle.11 Four patients received subsequent axillary or supraclavicular radiation; three of these patients had not received any previous radiation because they had a modified radical mastectomy. One patient had chest wall "boost" radiation. One patient had adjunct ovarian radiation. Four patients had anthracycline based chemotherapy. Six patients were treated with hormonal therapy (tamoxifen [5], anastrozole [1]) (Table 2). All of the patients who received tamoxifen had not received it before except one patient who had a 2-year treatment course. One patient received anastrozole because she had previously been treated with tamoxifen. Six patients received no systemic therapy after resection of their recurrence.


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  		TABLE 2. Treatment of the localized axillary recurrence
 
Outcomes
Five patients have died of disease, including all three patients who developed localized axillary recurrence within 2 years of treatment for primary breast carcinoma. Four patients are alive with disease, two patients have distant disease (spinal cord and bone or ovary metastases), two patients have local disease (subcutaneous chest wall nodules and axillary mass or supraclavicular fossa disease). Six patients are currently disease free, including one patient who had a third axillary dissection for a second localized axillary recurrence. One patient who is disease free has significant lymphedema. Ten-year overall actuarial survival is 56% (Fig. 1).



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  		FIG. 1. Overall survival.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Isolated axillary recurrence is an uncommon event after previously adequate (level I and II) axillary surgery.2,4,12–15 In retrospective case series, the incidence of LAR after prior axillary surgery ranges between 0.5% and 3%.2,4,12–14,16 It has been shown that as fewer lymph nodes are removed as part of a level I, II axillary dissection, the probability of axillary recurrence increases.17 If patients are treated with a mastectomy alone (no axillary component), then recurrence rate in the axilla is as high as 17% to 19%.18,19 Currently, estimates for the number of lymph nodes to retrieve for an adequate level I or II axillary lymph node dissection range between 8 and 15.20–22

Significant morbidity can be associated with an axillary recurrence. McKinna et al.19 report on 38 patients with isolated axillary recurrence of whom 21 developed symptoms: lymphoedema,16 pain in arm or hand,11 and sensory or motor changes.7 Even with treatment, a minority of the patients with severe symptoms gained control of their pain, lymphedema or sensory and motor changes before their death or last follow-up. In addition, approximately 50% of patients who develop ipsilateral axillary recurrence will have evidence of metastatic relapse and a life expectancy limited to a few years.19,23

With the emergence of sentinal lymph node biopsy, it could be anticipated that the incidence of LAR will increase because this technique has an associated 5% to 15% false-negative rate in multi-institutional series.5–8 In addition, many surgeons perform fewer completion axillary lymph node dissections after SNB when they are learning this new technique than is currently recommended (20–30), which could also increase the number of false-negative results.9,10 Hence, even in the upcoming era of sentinel lymph node biopsy, LAR, with its associated morbidity and increased risk for metastatic disease, will continue to be a clinical scenario that surgeons will face in their practice.

Some groups have suggested that patients with a positive SLN may not require a standard level I or II axillary lymph node dissection. In particular, suggestion is that patients with small primary breast carcinomas (T1, T2) and isolated cellular metastases, micrometastases (<2 mm) or metastases only identified with immunohistochemical staining can be offered the option of avoiding an axillary dissection.24,25 Guenther et al.25 reports on a cohort of 46 women with small (mean 1.65 cm)cancers of the breast who were identified to have metastases in the SLN, but who did not go onto axillary lymph node dissection.25 In this cohort, 16 positive SLN were seen on hematoxylin-eosin staining and 30 SLN were identified from positive immunohistochemical staining. At a mean follow up of 32 months, no axillary recurrences were identified. Despite these findings, our group advocates a standard level I or II axillary lymph node dissection be performed after a sentinel node, examined with hematoxylin-eosin staining, is found to harbor metastases. An ongoing American College of Surgeons Oncology Group trial (Z011), however, has been designed to determine the therapeutic value of a completion axillary dissection after a positive sentinel node biopsy.

In our study, only isolated axillary recurrences amenable to curative intent surgery were included. Interestingly, two of the patients who were thought to be node negative at initial axillary dissection were found to have an undissected arch at their second dissection that harbored their recurrent or residual disease.11 This arch is well described in anatomy texts26 and is present in 7% of the population.27 It is found at the lateral border of the axilla, and lymph nodes are invariably found beneath it. Since the advent of the sentinel node biopsy, it is often possible to track radiocolloid to a node in this section. The oncologic significance of this anatomic variation is that sentinel nodes or nodes with metastases can lie undetected and unresected beneath the muscle fibers, which can ultimately result in the patient’s cancer being under staged. This emphasizes that an adequate axillary dissection, including number of lymph nodes retrieved and identifying anatomic areas where lymph nodes can be found, must be completed at the initial surgery to minimize the risk of axillary recurrence.11,17

In our study, despite further surgery, the three patients who developed LAR within 2 years of their initial diagnosis of breast cancer did poorly. The average age of these patients was 42 years. None of these patients received adjuvant chemotherapy (one refused, one was treated with tamoxifen and one patient had a change in the pathologic diagnosis of carcinoma and chemotherapy was terminated). Early recurrence (<2 years) and young age previously have been reported as negative prognostic factors.1,16 It is not clear if the addition of systemic chemotherapy in this small group of patients would have changed their disease course. Seven of the 10 surviving patients from our cohort did receive chemotherapy after the treatment of their primary breast carcinoma (average age 48.5 years at time of first diagnosis). Of the 3 surviving patients who did not receive chemotherapy, 1 was treated in 1969 for her initial breast carcinoma and the other 2 patients were 62 and 64 years of age at the time of their primary diagnosis.

Five-year survival after LAR is diminished, 39% to 50% at 5 years.3,4,16 Our overall actuarial survival at 10 years was 56%. This suggests that patients can be long-term survivors after LAR if their disease is amenable to surgery and aggressive adjuvant treatment. Our finding corresponds with that of Newman et al.23 who describe a cohort of 30 patients with isolated axillary recurrence who were treated with multimodal therapy including a surgical component (median follow-up 70.8 months). Distant metastases developed in 50% of this cohort and were more likely in cases of an uncontrolled axillary recurrence. A controlled axillary recurrence was more likely when patients received a combination of surgery, radiation, and chemotherapy compared with single or dual modality therapy (94% vs. 36% vs. 69%, P = .005).23


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
We suggest that LAR may well increase with the growing use of SNB. Consequently, knowledge of how to treat localized axillary recurrence is relevant to current practice. In this study, patients with surgically amenable LAR were treated with an individualized multimodal treatment plan that included surgery. Patients who had a short (<2 year) disease-free interval and were young did poorly. It is not clear if receiving chemotherapy would have changed the disease course in these patients. However, patients with a disease-free interval of >2 years who had a complete surgical eradication of LAR and adjuvant treatment, had an overall survival that was better than has been previously reported. Clinical trials to determine the best adjuvant treatment for patients with LAR who have disease amenable to surgery would be beneficial, although small numbers of patients can limit the feasibility of such trials in a single institution setting.


   ACKNOWLEDGMENTS
 
ACKNOWLEDGMENTS

The authors thank Linda Last for her help with manuscript preparation.

The acknowledgments are available online at www.annalssurgicaloncology.org.


   FOOTNOTES
 
In the era of sentinel node biopsy, localized axillary recurrence (LAR) may have increased relevance. We assessed survival outcomes in women with LAR.

Received for publication January 22, 2003. Accepted for publication August 5, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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