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10.1245/ASO.2006.05.015
Annals of Surgical Oncology 13:501-507 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Axillary Ultrasonography to Detect Recurrence After Sentinel Node Biopsy in Breast Cancer

Howard C. Snider, Jr., MD1, Eva Rubin, MD2 and Rebecca Henson, RN1

1 Department of Surgery, Baptist Medical Center, 2105 E. South Boulevard, Montgomery, Alabama 36116
2 Department of Radiology, Baptist Medical Center, 2105 E. South Boulevard, Montgomery, Alabama 36116

Correspondence: Address correspondence and reprint requests to: Howard C. Snider, Jr., MD; E-mail: hsnidermd{at}pol.net.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Sentinel node biopsy (SNB) for breast cancer has a false-negative rate of approximately 5%. Initial reports of follow-up show lower axillary recurrence rates than expected. We performed axillary ultrasonography to determine whether occult recurrences could be detected.

Methods: In a community hospital setting, 289 patients who had SNB for breast cancer in a single surgeon’s practice underwent axillary examination by the surgeon followed by axillary ultrasonography by a dedicated breast radiologist. Ultrasonography was performed one time from 4 to 79 months (median, 25 months) after surgery. Five patients with suspicious nodes had ultrasound-guided fine-needle aspiration, and one had a core biopsy.

Results: No patient had suspicious nodes on clinical examination. Only six patients had ultrasound findings that warranted intervention. Five patients had benign cytological characteristics, and one had a benign core biopsy result. No evidence of axillary recurrence was found in any patient.

Conclusions: Axillary ultrasonography did not detect occult metastases in any patient and is not recommended for routine follow-up after SNB. The lack of ultrasound evidence of metastasis suggests that the recurrence rate is likely to remain low.

Key Words: Sentinel node • Ultrasound • Axilla • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
For the entire 20th century, the standard treatment of patients with breast cancer included an axillary lymph node dissection (ALND). Initially the procedure was performed in an attempt to eradicate loco-regional disease and, it was hoped, to improve survival. In the last quarter of the century, the status of the axillary nodes became an important determinant of the need for adjuvant therapy in the form of chemotherapy or hormonal manipulation. ALND, however, is accompanied by a significant risk of unpleasant side effects: most notably numbness, paresthesias, and lymphedema. Sentinel node biopsy (SNB) was introduced a decade ago by Krag et al.,1 who used a gamma probe–directed approach, and by Giuliano et al.,2 who used a vital blue dye for identification of the sentinel node. Albertini et al.3 used a combination of radioactive tracer and blue dye that was later shown to be more accurate than either method used alone.4 Multiple early studies, including our own, demonstrated that SNB accurately reflects the status of the entire nodal basin.3–6 SNB rapidly became popular and is now considered the preferred method of axillary staging for surgeons who are experienced with the procedure.7

SNB is known to have a significant false-negative rate. One large multi-institutional study showed the false-negative rate to be 11.4% overall, and rates for individual surgeons in the study ranged between 0% and 29%.8 A large single-institution study showed false-negative rates to range between 7% and 33% for individual surgeons. Even experienced surgeons in that study had false-negative rates as high as 20%.9 A meta-analysis of 13 published reports indicated that overall the false-negative rate is 5.1%.10 Early reports of axillary recurrence after SNB showed failure rates to be lower than one would expect from the previously reported false-negative rates.11–18 In these studies, patients were followed up only with mammography and physical examination. Mammography does not include the entire axilla and is not a reliable way to follow up patients for axillary recurrence. Physical examination of the axilla is notoriously unreliable, with reported false-negative rates as high as 35% to 39%.19–21 Ultrasound evaluation of the axilla has been shown to detect nodal metastases earlier than physical examination in undissected nodal basins in patients with melanoma.22

After one of us (H.C.S.) had been performing SNB alone without ALND for >5 years for clinically node-negative patients, no axillary recurrences had been detected. Because some of our patients with positive sentinel nodes declined completion ALND, we hypothesized that some patients had undetected axillary metastases that might be detected with ultrasonography. We report herein the institutional review board–approved study we performed to determine whether axillary ultrasonography in asymptomatic patients after SNB for breast cancer would detect unsuspected recurrences.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
After establishing the accuracy of SNB with completion ALND, one of us (H.C.S.) began performing SNB without ALND in 1997 for patients with clinically negative axillae. Patients with clinically positive nodes and some with extensive or multicentric disease continued to undergo ALND without SNB. Most patients during the study period had preoperative axillary ultrasonography. Patients who had suspicious nodes on ultrasonography underwent fine-needle aspiration (FNA) for cytological analysis. When metastasis was confirmed, the patients underwent ALND without SNB. Three hundred ninety-five patients with clinically (and usually sonographically) negative axillae underwent SNB between December 1997 and September 2004 (the total SNB population). Fifty-eight of those patients had immediate or delayed ALND when axillary metastasis was confirmed by touch preparation, frozen section, or permanent section analysis. Those patients did not have axillary ultrasonography and are, therefore, not part of the primary study population. Patients in whom a sentinel node could not be found usually underwent ALND. Three patients in whom the sentinel node could not be found did not have ALND and are included in the study population. Beginning in June 2003, patients were invited to participate in the institutional review board–approved study at the time of their regularly scheduled office visit. After giving informed consent, patients had a careful clinical assessment of the axilla by the surgeon (H.C.S.) and were then scheduled for axillary ultrasonography by an experienced breast radiologist (E.R.). An attempt was made to contact patients who did not come in for follow-up during the ensuing year to encourage them to participate in the study. Seven patients who had SNB died, 20 were lost to follow-up, and 21 declined to participate in the study; this left 289 for analysis (the primary study group). One hundred six patients had SNB but did not have ultrasonography for the reasons listed previously.

Patients ranged in age from 33 to 88 years (mean, 62 years). Forty-seven patients with ductal carcinoma-in-situ only and 242 patients with infiltrating carcinoma were evaluated with one axillary ultrasound examination at some point during their follow-up. Infiltrating tumors ranged in size from less than a millimeter (microinvasion) to 7 cm (mean, 1.2 cm). Of the infiltrating carcinomas, 212 (88%) were infiltrating duct carcinomas, both not otherwise specified and special types, and 30 (12%) were infiltrating lobular carcinoma. SNB was always performed with 99mTc sulfur colloid and usually with blue dye (either isosulfan or methylene blue) as well. Injection of 99mTc was intradermal in 193 patients (67%), peritumoral in 74 (26%), subareolar in 9 (3%), and not recorded in 13 (4%). Injection of blue dye was subareolar in 182 patients (63%), peritumoral in 52 (18%), and not used or not recorded in 55 (19%). The number of sentinel nodes (radioactive, blue, or palpable) removed ranged from 0 to 8 (mean, 2.3). Fifty patients (17%) had mastectomies, and 239 (83%) had partial mastectomies. Follow-up was measured from the time of SNB until axillary ultrasonography and ranged from 4 to 79 months (median, 24 months) for patients with invasive carcinoma and from 5 to 69 months (median, 31 months) for patients with ductal carcinoma-in-situ.

Patients who had positive sentinel nodes in whom an exact measurement of the metastasis was not given in the pathology report had their slides reviewed by a pathologist. The size of the largest sentinel node metastasis was measured with an ocular micrometer and recorded. Node-positive patients also had their charts and films reviewed by a radiation oncologist to determine whether any modification of the usual ports had been made and the percentage of the axilla that was included in the radiation field.

Sonography of the axillary and internal mammary nodes was performed in all patients by using an ATL HDI 5000 ultrasound unit (Philips/ATL, Bothell, WA) with a 12-5 transducer and compound scanning. The axilla was scanned from several centimeters below the axillary scar resulting from the SNB to the highest level reachable with the transducer. Scanning was performed in transverse overlapping sweeps with the transducer held in the sagittal or radial plane and in overlapping sagittal sweeps with the transducer held in the transverse or antiradial plane. Scanning included the axillary tail and upper outer quadrant for identification of abnormal intramammary nodes, if present.

A node was considered to have been identified if it could be clearly seen in orthogonal planes. Axillary nodes were considered to be abnormal if they were abnormal in shape (nonreniform, round, or irregular), were unusually hypoechoic, lacked all or part of the hilus, or had irregular cortices, particularly nodular protrusions of the cortex. Size was not used as a criterion—many of our patient population had very large predominantly fatty nodes.

If no axillary nodes were identified, the axilla was rescanned with compound scanning turned off and color Doppler imaging on. A paired artery and vein were sought entering what seemed to be a hilus. When found, the node was verified with compound scanning in orthogonal planes.

The internal mammary area was scanned with transverse sweeps in the sagittal plane from the second to the sixth interspace. Transverse scans were performed only if an abnormal node was thought to be present. Internal mammary nodes were considered abnormal if they measured ≥5 mm in diameter. Patients who had normal or benign-appearing findings were returned to routine follow-up that did not include further axillary ultrasonography. Patients with indeterminate or suspicious nodes underwent interval follow-up, FNA for cytological analysis, or core biopsy by the radiologist.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
None of the patients was thought to have suspicious axillary lymph nodes on physical examination. Only six patients (2%) had findings on ultrasonography that were considered at least mildly suspicious for malignancy and necessitated either follow-up or intervention. One patient (.4%) had elongated, minimally suspicious nodes that remained stable on interval follow-up and did not require sampling. Three patients (1.1%) underwent FNA for mildly suspicious axillary foci. One of them had a 1.4-cm irregular hypoechoic mass with increased vascularity 5 months after SNB. FNA showed only adipocytes and leukocytes. Another had 5-mm rounded, hypoechoic nodes that persisted on 6-month follow-up. FNA at that time showed benign lymphoid cells. The third patient had one slightly enlarged node with a cortex that was more hypoechoic than usual. FNA showed a small group of benign lymphocytes. One patient (.4%) had a core biopsy of a 6-mm rounded, hypoechoic focus with increased vascularity 68 months after SNB. The biopsy showed only reactive hyperplasia. One patient (.4%) had normal axillary nodes but a 7-mm irregular, nodular focus with increased vascularity in the ipsilateral internal mammary chain. The finding persisted at 6-month follow-up, at which time FNA showed peripheral blood with no evidence of malignancy. No patient had evidence of malignancy on FNA or core biopsy.

Forty-two patients had some tumor deposits in their sentinel lymph nodes. Twenty-eight had standard radiation or no radiation at all, and 14 had the usual ports modified to include more of the axilla. Six of the 42 patients had deposits that would now be considered node negative because they were <.2 mm in diameter. One of those six patients had chest wall radiation ports extended to include 80% of the axilla and the supraclavicular nodes. The other five had either standard radiation or none at all. Thirty-six patients were truly node positive. Their nodal status and locoregional and systemic treatments are listed in Table 1Go.


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  		TABLE 1. Number of nodes, size of metastasis, and treatment of patients with node-positive infiltrating carcinoma who did not have ALND
 
Nine patients had mastectomies. Two of the nine had radiation ports modified to include all of the axilla, and the third had 80% of the axilla radiated through standard ports. Six patients elected no radiation for a variety of reasons, including age, fear of lymphedema, and small tumor deposits thought to have a low risk of residual disease. In the early years of the study, we accepted pathologic descriptions such as "a small focus; a single aggregate of a few cells; four or five cells" to describe sentinel node metastases. Upon later review, some of the tumor deposits, when measured with an ocular micrometer, were larger than originally thought. We now insist on an exact measurement of the size of the largest nodal metastasis. Of the 27 node-positive patients who had partial mastectomies, 1 refused radiation, 16 had standard ports, and 10 had ports extended to include more of the axilla. Even in the patients who had standard ports, the axilla was estimated to be completely covered in 5 (31%) of 16. The others had 20% to 90% of the axilla radiated. When the ports were modified, 9 (90%) of 10 had 100% coverage, and 1 had 80% of the axilla included.

One patient who had a partial mastectomy had a tumor deposit almost 2 mm in size in one of three sentinel nodes but refused all forms of adjuvant therapy, including breast radiation, chemotherapy, and tamoxifen. She had a normal axillary ultrasound examination as a part of this study 18 months after SNB. Recently she developed an ipsilateral breast lesion recurrence 38 months after her original operation. Repeat axillary ultrasonography results were again normal. Because of the 3-year interval without axillary recurrence, she elected to have repeat SNB instead of ALND. Two sentinel nodes were removed and were histologically normal.

None of the six node-positive patients who had mastectomy without radiation has had a relapse after a mean follow-up of 32 months (range, 9–57 months). None of the 36 node-positive patients had any axillary abnormalities detected on ultrasonography. One patient who had a few immunohistochemically positive epithelial cells in her single sentinel node (and is considered node negative) had the 6-mm rounded, hypoechoic node that was reactive on core biopsy.

Of the 395 patients who had SNB, 7 died, and 1 developed pulmonary metastasis without receiving axillary ultrasonography. None of them had clinically apparent axillary metastases at last follow-up. One patient who had a positive axillary node refused all forms of traditional treatment and elected to pursue alternative treatment with lifestyle modifications. She developed an ipsilateral breast lesion recurrence 6 years later and underwent re-excision. Repeat SNB (without preoperative ultrasonography) showed tumor in one of three sentinel nodes. Of the 242 patients with infiltrating carcinomas who had axillary ultrasonography, two had chest wall recurrence, one developed ipsilateral breast recurrence, three developed contralateral breast primary tumors, and one developed pulmonary metastasis. One patient developed contralateral but not ipsilateral nodal metastasis. None of them had clinically or sonographically apparent ipsilateral axillary metastases.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
As we gained experience after our initial report of SNB and completion ALND, our ability to find the sentinel node improved. Initially we were able to find the node 85% of the time by using a peritumoral injection of 99mTc without blue dye.6 With the publication of reports that subareolar blue dye injection was accurate and that a combination of 99mTc and blue dye was more accurate than either technique alone, 4,23,24 we added subareolar dye. After reports of intradermal injection of 99mTc,25–27 we abandoned peritumoral injection and have been able to find the sentinel node 99% of the time for the last few years with the combination of intradermal 99mTc and subareolar blue dye. With the publication of reports of the accuracy of SNB in multicentric disease,28,29 we have now eliminated ALND in our practice for node-negative patients.

During the entire study period, we have used axillary ultrasonography to preoperatively identify positive axillary nodes and have been able to go straight to ALND in several patients in whom metastasis was confirmed by FNA and, more recently, core biopsy. Others have confirmed the clinical usefulness of preoperative axillary ultrasonography. Yang et al.30 evaluated patients before surgery with axillary ultrasonography and compared the results with the pathologic findings at ALND, confirming an overall accuracy of 92%. Bonnema et al.31 detected metastases before surgery in 63% of node-positive patients by using ultrasound-guided FNA. Krishnamurthy et al.32 confirmed metastases before surgery in 93% of nodes with metastatic deposits >5 mm in diameter and in 44% of patients even when the deposits were <5 mm. Kuenen-Boumeester et al.33 used preoperative ultrasonography in patients with nonpalpable axillary nodes and detected metastases in 44% (37 of 85) by FNA; this represented 20% of the total patient population. Deurloo et al.34 confirmed metastases before surgery with FNA in 31% (37 of 121) of node-positive patients, and Sapino et al.35 did so in 56% (49 of 88). Oruwari et al.36 reported a sensitivity and specificity of 100% in 26 patients with locally advanced breast cancer who underwent preoperative staging with axillary ultrasonography and FNA. We have been able to eliminate some of the operative uncertainty where the planned procedure is dependent on intraoperative touch preparation or frozen section by identifying a subset of node-positive patients before surgery who never undergo SNB. We had a total of 336 patients with infiltrating carcinoma who had SNB (including 242 patients in the study, 58 who had ALND, and 36 patients with infiltrating carcinoma who declined to participate or were lost to follow-up). A total of 100 patients had tumor cells in their sentinel nodes, including the patients who had ALND, the 36 who were truly node positive but did not have ALND, and the 6 who had foci <200 µm and are now considered node negative. The 30% positivity rate (100 of 336) is lower than one would expect from the entire population of patients undergoing detailed pathologic evaluation of sentinel nodes obtained without pre-operative axillary ultrasonography because some patients went straight to ALND as a result of pre-operative FNA results.37

One weakness of our study is that 20 patients (5%) were lost to follow-up. It is possible that some of them developed recurrence that could have been detected with ultrasonography. The mean size of tumors was 1.2 cm both in patients who had ultrasonography and in those who were lost to follow-up. More importantly, 19 of the 36 node-positive patients who had ultrasonography had metastases larger than a millimeter. Although 5 of the 20 patients who were lost to follow-up had some tumor cells in their sentinel nodes, 3 patients had deposits <.2 mm and would be considered node negative, and another had a micrometastasis. Only one patient had a tumor deposit >2 mm in a sentinel node. Those patients who were lost to follow-up were observed from 1 to 51 months (mean, 21 months) and had no evidence of axillary recurrence before they were lost. We believe it is unlikely that the patients lost to follow-up would materially change the findings of the study. One patient who had a 2.5-mm focus in a sentinel node declined to participate in the study but is still under observation. She had no clinical evidence of recurrence after 25 months of follow-up.

All studies published to date have shown low rates of axillary recurrence after SNB. Chung et al.38 reported the highest failure rate to date (1.4%), with 3 axillary recurrences out of 208 breast cancers after a median follow-up of 26 months. Blanchard et al.39 had 1 recurrence (.1%) in 685 patients after a mean follow-up of 2.4 years. Other studies have shown no recurrences with follow-up as long as 39 months.11–14 Fant et al.18 reported no recurrences after a mean follow-up of 30 months in 36 patients who had positive sentinel nodes but who declined ALND. Guenther et al.17 reported no recurrences after a median follow-up of 32 months in 46 node-positive women who declined ALND. Reitsamer et al.40 followed up patients not only clinically, but also with axillary ultrasonography, every 3 months. They found no recurrences in 116 node-negative patients after a mean follow-up of 22 months. In 614 patients, 11% of whom were node positive, Jeruss et al.41 found only 1 recurrence (.15%) after a median follow-up of 27.5 months. Smidt et al.42 found 2 recurrences (.46%) in 439 patients after a median follow-up of 26 months. Naik et al.43 recently published a large series from Memorial Sloan-Kettering Cancer Center. With a median follow-up of 31 months, only 10 (.25%) of 4008 patients had experienced an axillary recurrence. In the 210 node-positive patients in the series that underwent SNB without ALND, there were only 3 (1.4%) recurrences, even though half of those patients had no special attempt to include the axilla in the radiation ports. It has been previously shown that the area of the sentinel node is included in standard breast radiation ports in 94% of patients,22 and with slight modifications, 80% of levels I and II are included.44 Nevertheless, if the surgeon depends on radiation oncologists to treat possible residual disease in the axilla, we believe it is imperative that there be close communication between the two to determine the extent of axillary treatment necessary.

All of these studies suggest that the rate of axillary recurrence after SNB will remain lower than expected from the reported false-negative rates. Because we are able to routinely identify and perform biopsies of subcentimeter axillary metastases before surgery with ultrasonography guidance, we believe it is unlikely that a large number of nodal metastases destined to become clinically significant escaped detection in this study. It is our contention that the rate of axillary recurrence in most series will likely remain well below the published false-negative rates. Unfortunately, the American College of Surgeons Oncology Group trial Z0011, which was designed to answer the question of how to manage the axilla in node-positive patients, closed because of a lack of accrual. We may never have an answer to that question from a randomized trial. Considering the low rate of axillary recurrence even in SNB-positive patients who do not have ALND, it is possible, with the maturation of current studies and the addition of other nonrandomized trials, that enough data will accumulate to allow SNB without ALND even in some patients who are node positive, thus substantially reducing morbidity without compromising survival. We have found the Memorial Sloan-Kettering Cancer Center nomogram (available online at http://www.mskcc.org) for estimating the likelihood of additional positive nodes to be useful in counseling patients.45 Until more data are available, we believe that patients should make informed decisions, with the help of their physicians, as to how they want their axillae to be managed. For the time being, we believe that most, but not all, patients should have ALND or radiation when positive nodes are found on SNB. We continue to use preoperative axillary ultrasonography to identify patients who should have ALND, but we do not believe that routine axillary ultrasonography after SNB is useful for most patients.


   ACKNOWLEDGMENTS
 
The authors thank Chad Bianci, Katelyn Braswell, and Richard Conely for their excellent help in contacting patients and gathering data; Kathy Dorman for her expert assistance in preparation of the manuscript; Mike Bridger, MD, and Glen Pinkston, MD, for reviewing the sentinel node slides and providing accurate measurements of the metastases; Bill Helvie, MD, Steven Stokes, MD, Wes Glisson, MD, Bill Hixon, MD, and Tom Beatrous, MD, for evaluating the percentage of the axilla that was treated in their ports; and Lee Franklin, MD, for his invaluable help in reviewing numerous patient films and records to determine the axillary coverage.

Received for publication June 8, 2005. Accepted for publication October 21, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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