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Analysis of Sentinel Lymph Node Mapping With Immediate Pathologic Review in Patients Receiving Preoperative Chemotherapy for Breast Carcinoma

From the Divisions of Surgery (ARM, VET, JS, MSK, ABC), Pathology (AA, I-TY, FES), and Radiology (PMO, CM, WTP), University of Texas Health Science Center at San Antonio, Texas.

Correspondence: Address correspondence and reprint requests to: Alexander R. Miller, MD, Department of Surgery, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78229; Fax: 210-567-6862; E-mail: millerar{at}uthscsa.edu

	ABSTRACT

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Background: Sentinel lymph node mapping (SLNM) and neoadjuvant chemotherapy are becoming established components of therapy for selected patients with breast carcinoma. However, neoadjuvant therapy has been considered a relative contraindication to SLNM. In an effort to learn whether patients who have received preoperative chemotherapy can undergo accurate SLNM, we evaluated our experience with this technique.

Methods: From January 1997 to June 2000, SLNM and axillary lymph node dissection were concurrently performed in 35 patients who received preoperative chemotherapy. Mapping was performed with ^99mTc sulfur colloid only in one patient and Lymphazurin dye only in 15 patients, and the two methods were combined in the remainder.

Results: SLNM successfully identified a sentinel lymph node in 30 (86%) patients. Metastatic disease was identified in the sentinel lymph nodes of four patients during surgery. The intraoperative pathologic diagnosis proved to be correct in 19 (79%) of 24 patients. The final pathologic diagnosis of the sentinel lymph node reflected the status of the axillary contents in all patients in whom it was identified.

Conclusions: These results demonstrate that SLNM can be consistently performed in patients receiving preoperative chemotherapy for breast cancer, suggesting the utility of this technique in this patient population.

Key Words: Breast cancer • Sentinel lymph node mapping • Neoadjuvant chemotherapy • Axillary lymph node dissection

	INTRODUCTION

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Sentinel lymph node mapping (SLNM) was first described in 1992 for patients with clinical stage I cutaneous melanoma and has since become the standard method of regional staging for this disease.¹ Krag et al.² first applied SLNM to breast carcinoma in 1993, using injection of ^99mTc sulfur colloid (^99mTc-sc). In 1996, Albertini et al.³ described the combined use of ^99mTc in addition to Lymphazurin^TM (isosulfan blue; US Surgical, Norwalk, CT) dye for SLNM of breast cancer patients. At present, the utility of SLNM is being evaluated in the local therapy and staging of breast carcinoma in patients with a clinically negative axilla. SLNM seems to be replacing elective axillary lymph node dissection because of the minimal morbidity and high level of accuracy associated with this procedure.^4–7 When SLNM is performed by an experienced team using serial sectioning and immunohistochemical evaluation, it is as accurate as axillary lymph node dissection in determining nodal status.^3,8–14

As the utility and efficacy of preoperative chemotherapy for breast cancer is being demonstrated,^15,16 investigators have considered the appropriateness of SLNM in this patient group. To date, variable data have been generated regarding SLNM in patients undergoing neoadjuvant chemotherapy, and such patients have been excluded from multicenter SLNM protocols. Recent reports have suggested that SLNM may not be accurate in this patient population and that thus perhaps it should not be attempted.¹⁷ Because our group selectively uses neoadjuvant chemotherapy in the treatment of breast cancer, we were eager to determine whether SLNM could be accurately performed in this patient population. To critically answer this question, we initiated an institutional protocol in which patients receiving preoperative chemotherapy underwent concurrent SLNM and axillary lymph node dissection to fully stage the axilla and rule out the possibility of undetected disease. Our data suggest that this technique can be accurately performed in the majority of patients and that cytopathologic review by experienced pathologists can correctly stage disease during surgery in many cases, thus avoiding unnecessary surgical dissection and reducing the number of patients who require reoperation for axillary clearance.

	MATERIALS AND METHODS

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Patients
From January 1997 through June 2000, SLNM and concurrent axillary lymph node dissection were performed in 50 patients as a means of breast cancer staging. Thirty-five patients received preoperative chemotherapy, either as part of a national protocol designed to evaluate the efficacy of this therapy for early-stage breast carcinoma (National Surgical Adjuvant Breast and Bowel Project B-27; n = 31) or outside the context of a protocol. Protocol-treated patients received a chemotherapeutic regimen consisting of four cycles of doxorubicin and cyclophosphamide (25 patients), alone or followed by four cycles of docetaxel (6 patients). Patients treated off-protocol underwent doxorubicin-based therapy consisting of four cycles administered before surgery. When this plan was initiated, SLNM was used in the context of an institutional review board-approved protocol for breast carcinoma that allowed participation by patients receiving preoperative chemotherapy. At the time of presentation for surgery, all patients with unifocal tumors and clinically negative axillae were queried regarding their desire to undergo SLNM with concurrent axillary lymph node dissection. All patients who agreed to this plan provided their informed consent for the procedures used.

Methods of Mapping
Patients who received ^99mTc-sc were treated as follows: palpable tumors were subjected to four-quadrant intraparenchymal injection of unfiltered ^99mTc adjacent to the tumor (2-ml volume; .250 mCi per quadrant) by the surgeon. All nonpalpable tumors were intraparenchymally injected in four quadrants after radiologically guided needle localization by the radiologist. Lymphazurin injection (3–5 ml) was performed by the surgeon 5 minutes before the axillary incision. Palpable tumors were injected in four quadrants intraparenchymally around the tumor. Nonpalpable tumors were injected in four quadrants around the needle localization wire without additional radiological guidance. Navigator^TM (US Surgical) and C trak^TM (Care Wise, Morgan Hill, CA) handheld gamma probes were used to map the sentinel lymph node (SLN) 2 to 6 hours after injection. Sentinel node identification was made on the basis of observing a blue node or lymphatic draining from a lymph node, or observing gamma counts more than three times the background within the node. Lymph nodes were sent for immediate pathologic review in 24 cases. Complete axillary dissection followed SLNM. In cases in which ^99mTc-sc was injected, the axilla was reprobed after axillary dissection, and the excised axillary contents were also probed to ensure that SLNs were not missed.

Methods of Histological Evaluation
Immediate Tissue Processing
SLNs were immediately delivered to the pathology laboratory and were entirely submitted for pathologic examination. After sectioning, cytological preparations were made of the cut nodal surface on glass slides by touch preparation technique or scraping. Slides were air dried and stained with Diff-Quik^TM (Dade Behring, Deerfield, IL), alcohol fixed and stained by hematoxylin and eosin (H&E), or both of these. Pathologic analysis was based on standard cytological criteria. Frozen section was performed by embedding one half of the lymph node in OCT^TM and Tissue-Tek^TM (Sakura, Torrance, CA). Quick freezing was performed with Histobath II^TM (Shandon Lipshaw, Pittsburgh, PA), and frozen sections (4 µm thick) were cut on a cryostat. Frozen sections were stained with H&E, and histological evaluation was performed. The method of intraoperative SLN preparation was determined on the basis of the preference of the responsible pathologist. Fourteen patients had cytological examination of sentinel nodes, seven cases were subjected to frozen section analysis, and three cases were examined both cytologically and by frozen section.

Final Tissue Processing
All remaining SLN tissue was fixed in neutral buffered formaldehyde and processed in paraffin blocks. Sentinel nodes were serially sectioned at 2-mm intervals if they were 4 mm or more in diameter, and they were bisected if they were <4 mm. One to six blocks were examined in each patient, representing one to five sentinel nodes. If the initial H&E section was negative for metastatic disease, two additional H&E levels were examined on each block, and an immunohistochemical stain for keratin (AE1) was performed. Nineteen cases were also examined by keratin AE3 antibody as well. Negative controls were performed in each case.

	RESULTS

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Demographic Data
The median tumor size was 3.5 cm (range, .8–10 cm) before chemotherapy, as determined radiologically (ultrasound or mammography), and was 1.1 cm (range, 0–3.5 cm) at the time of surgery, on the basis of gross pathologic analysis. Patients were treated with a median of 4.6 cycles of chemotherapy (range, 3–8 cycles). Ten patients underwent mastectomy, and 25 patients were treated with breast-conserving surgery. Nineteen patients with nonpalpable tumors undergoing lumpectomy required needle localization.

SLNM Techniques and Technical Success
SLNM was performed by using only ^99mTc-sc in one patient (2.9%) who had an allergy history. Ten patients were mapped with Lymphazurin dye only (29%) because of logistical difficulties encountered early in the study, and the remaining 24 individuals (69%) were mapped with Lymphazurin plus ^99mTc-sc, our current institutional technique. Before the incision, 19 patients had hot spots identified with a handheld gamma probe. SLNs were identified in 30 individuals (86%). In two of the five unsuccessfully mapped patients, Lymphazurin dye was the only mapping agent used, whereas the other three cases used ^99mTc-sc and Lymphazurin dye. Tumor size did not seem to be a factor affecting the success of mapping, because the tumor size of these five cases ranged from 1.2 to 3.2 cm, nor did the type or amount of chemotherapy (range, 4–8 cycles) provided before surgery. A total of 75 SLNs were identified (2.14 per patient; range, 0–5).

Pathologic Analysis of SLNs
Lymph nodes were submitted for immediate pathologic review in 24 cases and were subjected to only final review in 6 cases, for which an experienced pathologist was unavailable or there was miscommunication with operating room personnel. Final pathologic review identified one false-positive result and four false-negative results and confirmed the intraoperative diagnosis in 19 cases (79%). The false-positive result occurred because of interpretive error of a cytological preparation. Two of the false negatives were based on cytological preparations in which rare malignant cells were not observed during the intraoperative review. In the other two cases, no tumor cells were present in the preparations made at the time of intraoperative review but were present on deeper sections made for final diagnosis (sampling error). The sensitivity of immediate pathologic review was 43%, and the specificity was 94%.

Nine patients who underwent successful SLNM were ultimately found to have metastatic tumor in lymph nodes. The SLN was the only positive node in four of these cases (Fig. 1). One patient who was not successfully mapped also displayed metastasis. Metastatic tumor was identified in four cases at the time of intraoperative review, and two additional cases were identified at the time of review of final H&E sections. Three cases showed metastatic disease only in immunohistochemical preparations. One of these was considered to demonstrate only lymph node scarring at the time of intraoperative pathologic evaluation.

View larger version (14K): [in this window] [in a new window]   FIG. 1. Flow diagram detailing pathologic findings of patients undergoing sentinel lymph node (SLN) mapping. IHC, immunohistochemical analysis for cytokeratin.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The appropriate role of SLNM in patients with breast cancer has not yet been defined. In the setting of melanoma, SLNM has become the standard of care for selected patients on the basis of multiple controlled evaluations. Initial studies have suggested that SLNM may be accurately performed in breast cancer patients with small primary tumors and clinically negative axillae.^7–14 However, some authors have concluded that patients receiving preoperative chemotherapy should not undergo SLNM.¹⁷ These individuals observed that the accuracy of mapping was diminished, presumably because of lymphatic scarring from systemic therapy. Because our institution has widely used neoadjuvant chemotherapy to locally downstage patients, we believed that it was important to determine whether SLNM could be accurately performed in this expanding patient population. Furthermore, we sought to determine whether immediate pathologic analysis could accurately determine the status of the axilla during surgery, thus reducing the need for subsequent surgical procedures required to treat regional metastatic disease.

In our experience, SLNM was successfully performed in more than 85% of patients who received neoadjuvant chemotherapy. This success rate is equivalent to those of published reports involving patients who received no prior therapy for breast cancer and is consistent with a recent series describing SLNM in this particular patient population.^18,19 We were unable to identify an SLN in five patients. We did not find a difference in the ease of identifying a sentinel node as a function of what type of or how many cycles of chemotherapy patients received.

Multiple investigators have reported that advanced patient age increases the likelihood of unsuccessful mapping.^17,18 Indeed, four out of five of our unsuccessful mapping procedures occurred in postmenopausal patients. The remaining unsuccessfully mapped case occurred in an obese patient and was performed very early in our experience. Finally, three of the unsuccessfully mapped cases were performed by the surgeon least experienced in this technique. It has been well reported that technical errors in localization of SLNs are more commonly encountered in the initial stages of surgeons’ experience with this procedure.^20,21

In the patient group that was successfully mapped, the final pathologic status of the SLN reflected that of the remainder of the axilla in all 30 patients. Further, immediate pathologic analysis provided a specific means of intraoperative staging, although there were admittedly few histologically positive sentinel nodes in this series, and there were a significant number of initially negative cases subsequently identified to harbor micrometastatic disease. However, it is noteworthy that the reported sensitivity of 43% in this series compares favorably with other recent reports of SLNM in chemonaïve patients.²² In reviewing reasons for the inaccuracy of intraoperative pathologic diagnoses, we identified two interpretation errors. These cases, initially diagnosed as negative, were subsequently found to contain rare groups of malignant cells that were not accurately diagnosed by the pathologist at the time of touch preparation analysis. Two sampling errors accounted for the additional two false-negative cases. In one case of an initially positive diagnosis, subsequent review of the immediately analyzed preparation demonstrated that lymphocytes were misinterpreted as malignant cells. In all inaccurately diagnosed cases, initial diagnoses were not provided by the pathologists at our institution who were most familiar with SLN analysis. These findings emphasize the need for experienced pathologists to perform sentinel node evaluation and also illustrate the difficulty of histological interpretation of lymph nodes in patients undergoing neoadjuvant chemotherapy.

Presently, there is no consensus regarding the preferred method of intraoperative analysis of SLNs in patients with breast carcinoma.^23,24 Some investigators have suggested that touch preparation analysis is more accurate and specific when used for larger tumors.^25,26 Among our false-negative cases were two T1 tumors that manifested a complete clinical response to chemotherapy. We currently use a policy that only pathologists dedicated to SLN analysis review such cases. Each designated pathologist may select the method of analysis (touch preparation or frozen section) with which he or she is most comfortable.

It is critical to note the role of immunohistochemical analysis of SLNs. In three cases, or 10% of the successfully mapped patients in our series, cytokeratin staining proved to be the only method sufficiently sensitive to identify micrometastatic disease. Other investigators have also reported that immunohistochemical staining upstages approximately 10% of patients considered to have negative nodes on the basis of H&E analysis and is a critical component of SLN staging.^27–29 The ability to provide ultra-accurate staging information seems clinically relevant, because micrometastases in SLNs have been demonstrated to be the most significant factor associated with recurrence and overall survival.^24,27–31 This finding also seems true for patients who have received neoadjuvant chemotherapy.³²

It is important to note that there were no cases in which SLNs were identified remaining in the axilla or in the subsequently dissected axillary content, as judged by reprobing with the handheld gamma counter. This level of accuracy is favorable in comparison with other reported series of patients who did not receive neoadjuvant therapy, as well as a series of patients who did receive preoperative chemotherapy.^18,19 Although the clinical benefit of intraoperative pathologic assessment of sentinel nodes seems obvious, some investigators have questioned this practice as not being cost efficient, particularly for patients with small tumors whose sentinel nodes are less likely to contain metastases and in whom frozen section is less sensitive.²⁵ However, a consensus on this point has not yet been reached. Although not an element of data analysis, our internal analysis of resource utilization has estimated that this procedure costs approximately US$500 (including preparation and interpretation) and requires from 15 to 25 minutes to obtain results. Our institutional practice is therefore to perform such studies when an experienced pathologist is available. We are comfortable continuing this practice while indicating to patients that a possibility exists for revision of the intraoperative diagnosis after analysis of final histological preparations.

	Footnotes

 
Presented at the 54th Annual Meeting of the Society of Surgical Oncology, Washington, DC, March 15–18, 2001.

Received for publication August 27, 2001. Accepted for publication December 5, 2001.

	REFERENCES

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Miller, A. R. Articles by Cruz, A. B. Search for Related Content PubMed PubMed Citation Articles by Miller, A. R. Articles by Cruz, A. B., Jr Related Collections Chemotherapy Sentinel lymph node