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Right arrow Sentinel lymph node
Annals of Surgical Oncology 9:333-339 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Intraoperative Touch Preparation for Sentinel Lymph Node Biopsy: A 4-Year Experience

Ronda S. Henry-Tillman, MD, Soheila Korourian, MD, Isabel T. Rubio, MD, Anita T. Johnson, MD, Anne T. Mancino, MD, Nicole Massol, MD, LaNette F. Smith, MD, Kent C. Westbrook, MD and V. Suzanne Klimberg, MD

From the Fashion Footwear Association of New York/Virginia Clinton Kelley Research Fellowship (ATJ, LFS), University of Arkansas for Medical Sciences, Arkansas Cancer Research Center (ITR), Department of Veterans Affairs, Central Arkansas Veterans Healthcare System, Department of Surgery (RSH-T, ATJ, ATM, LFS, KCW, VSK) and Department of Pathology (SK, NM, VSK), Little Rock, Arkansas.

Correspondence: Address correspondence and reprint requests to: Ronda S. Henry-Tillman, MD, 4301 West Markham, Slot 725, Little Rock, AR 72205; Fax: 501-686-7861; E-mail: henryrondas{at}uams.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The optimal technique for intraoperative pathologic examination of sentinel lymph nodes (SLNs) is still controversial. Recent small series report sensitivity between 60% and 100% for various techniques. The aim of this study was to evaluate our long-term experience with touch preparation cytology (TPC) and frozen section (FS) in the intraoperative examination of SLNs for breast cancer.

Methods: A total of 247 patients with operable breast cancer underwent an SLN biopsy for staging of the axilla. The SLN was identified by 99mTc-labeled sulfur colloid unfiltered dye, blue dye, or both and dissected, and then intraoperative TPC or FS and permanent section, or both, were performed.

Results: A total of 479 SLNs were submitted for TPC and permanent hematoxylin and eosin. A total of 68 SLNs were positive by hematoxylin and eosin; 65 SLNs were positive by TPC, with a false-negative rate of 5.8%. The sensitivity for TPC was 94.2%, with a false-positive rate of 0.2%. A total of 165 SLNs were submitted for FS, with a sensitivity of 85.7% and a specificity of 98.6%. The false-positive rate was 1.4%, with a false-negative rate of 15.8%.

Conclusions: In a large series, TPC is as accurate as FS but is simpler and faster in the detection of intraoperative metastasis in SLNs for breast cancer.

Key Words: Sentinel lymph node • Breast cancer • Touch preparation cytology • Frozen section • Accuracy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sentinel lymph node (SLN) biopsy for breast cancer is approaching standard of care for staging the axilla in patients with early-stage breast cancer and clinically negative axillary lymph nodes. This technique has gained popularity supported by published data from numerous single-institutional and prospective multicenter trials, which have validated its accuracy in a wide variety of settings with a multitude of varied techniques.1–12

One of the many questions that surrounds the minimally invasive technique of SLN biopsy is how best to intraoperatively evaluate the SLN. That is to say, patients who benefit from a completion axillary lymphadenectomy (ALND) might have it performed at the time of the initial operation, thus eliminating the need for a second surgery.

The two most widely used techniques for intraoperative evaluation of SLNs for breast cancer are frozen section (FS) and touch preparation cytology (TPC). The reported sensitivities of these techniques range from 52% to 100% (Table 1).13–20 In the FS technique, the SLN is frozen and sectioned; one or two sections are mounted and stained, and the nodal architecture is examined for metastases. The sensitivity of the FS technique for breast cancer ranges from 11% to 25% for micrometastases and 90% to 100% for macrometastases.20 A second technique that is gaining popularity is TPC, or imprint cytology. In this technique, the SLN is bisected, and the cut surface is touched to a slide, stained, and examined for individual cells for metastases. On TPC, the morphology of neoplastic epithelial cells is distinctly different from that of the background lymphocytes and macrophages. The sensitivity of this method for the detection of micrometastases ranges from 90.9% to 100% (Table 1).14–16,21


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  		TABLE 1. Results of sensitivity and false-negative rates of intraoperative pathologic examination of the SLN
 
In 1998, Rubio et al.14 initially published our results of TPC for SLN on 55 patients, the sensitivity of which was 95.7% and the specificity of which was 100%. With the increasing use of SLNs for staging the axilla in breast cancer patients, a method that is reliable, fast, and accurate for intraoperative diagnosis is imperative. The aim of this study was to retrospectively review and evaluate our long-term experience with TPC and FS in the intraoperative evaluation of SLNs for breast cancer.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Patients diagnosed with breast cancer at the Arkansas Cancer Research Center and the University Hospital at the University of Arkansas for Medical Sciences from March 1996 to August 2000 were enrolled onto an institutional review board–approved clinical trial evaluating intraoperative TPC for SLNs. Enrollment criteria included operable documented invasive breast cancer (stage I and II; evaluated by fine-needle aspiration, core biopsy, or excisional biopsy) and clinically negative axillary lymph nodes. Patients with prior axillary operations or multiple primary tumors or who were pregnant were excluded from the trial.

Study Procedure
The technique for SLN biopsy used in this trial included either peritumoral or subareolar injection, performed as previously described by Krag et al.3 or Klimberg et al.,8 respectively. Patients were seen in the Nuclear Medicine Department on the morning of surgery. Each patient received a 4-ml injection containing 1.0 mCi of unfiltered 99mTc-labeled sulfur colloid diluted in saline injected in the peritumoral parenchyma or centrally in the subareolar plexus, but not into the tumor or the biopsy cavity. Localization with 99mTc ranged from 30 minutes to 8 hours after injection. Blue dye (Lymphazurin; US Surgical Corp., Norwalk, CT) was injected intraoperatively in the peritumoral parenchyma. A handheld gamma probe was used to localize the SLN separate from the zone of diffusion of the injection site. The supraclavicular fossa and the axillary and internal mammary lymph node chains were scanned for increased uptake. Counts were also taken over the right lobe of the liver to exclude intravascular injection. Areas of radiolocalization apart from this zone were deemed hot spots when counts were >10% of the background and corresponded to the underlying radiolabeled SLN. The SLNs were removed, and the wound was re-examined to ensure that all radiolabeled SLNs or blue nodes were identified and removed with the same technique. Ex vivo radioactivity of the removed SLN was measured, as was the bed count, to confirm that the SLN had indeed been removed. The patient then underwent either breast conservation surgery or mastectomy, with or without ALND.

Pathologic Evaluation
After dissection of the SLN, the specimen was sent fresh to pathology for TPC. The SLNs were sectioned at 2- to 3-mm intervals; those <2 mm were bisected. A slide was touched to the cut surface of the SLN, and the node was immediately placed in 95% ethanol. Hematoxylin and eosin (H&E) staining was performed to evaluate for metastases. All tissue was then submitted for permanent section, FS, or both on the discretion of the pathologist. This protocol has subsequently been discontinued to conserve tissue for permanent section, to recognize micrometastases on permanent section. The final 100 cases were evaluated by TPC. The results of the intraoperative TPC, FS, or both were reported to the operating room as negative for, suggestive of, or positive for cancer.

Statistical Analysis
Diagnostic accuracy, sensitivity, specificity, and positive and negative predictive values were calculated by using definitions given in Greenberg.22 Exact 95% confidence intervals (CIs) were obtained by using the software package StatXact3 for Windows (Cytel Software Corporation, Cambridge, MA).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patients
A total of 255 patients were enrolled onto this study. Eight patients with pure ductal carcinoma-in-situ were excluded from data analysis. These included patients with large areas of ductal carcinoma-in-situ who were, usually, undergoing a mastectomy. The mean age of the remaining 247 patients was 58.2 ± 12.6 years (range, 32 to 84 years). A total of 216 (87.4%) patients had infiltrating ductal carcinoma, 25 (10.1%) had infiltrating lobular carcinoma, and 6 (2.4%) were otherwise classified. The average tumor size was 1.99 ± 1.56 cm. More than half of the patients were classified as T1 (54%). Eight clinically staged T2 patients had tumors >5 cm on final pathology.

Study Procedure
The initial 60 patients underwent level I and II ALND after resection of the SLN, whether it was positive or negative, to document false-negative (FN) rates, and have been previously reported.4 In the remaining patients (n = 187), selective ALNDs were performed depending on the results of the SLN. A mean of 1.94 ± 1.5 sentinel nodes were removed per patient. If the SLN failed to localize, then a level I and II ALND was performed. If the SLN was negative, then ALND was not performed. ALND was performed on all patients with an intraoperatively positive TPC of the SLN.

Pathologic Evaluation
Intraoperative TPC analysis was used to evaluate 479 SLNs, and FSs were performed on 165 of these nodes. All nodes were subsequently reviewed on permanent serial section H&E. A total of 68 SLNs in 43 patients were positive for metastases on permanent H&E. Immunohistochemistry (IHC) was used selectively in patients in whom cells suggestive of cancer were identified on H&E. In two patients, micrometastases were confirmed. In both patients, the size of the micrometastases was <1 mm, and the correlating invasive tumor was a T1b lesion. Sixty-five SLNs were positive on TPC. There was a single false positive (FP) on TPC, with an FP rate of .2%, yielding a positive predictive value of 98.5% (95 CI, 91.8%–99.9%; Table 2). There were four FNs on TPC, yielding an FN rate of 5.8%; three of these contained micrometastases. On final H&E and review of the TPC, the focus of carcinoma present on permanent section was <1 mm in greatest dimension in all three cases. The fourth FN was believed to be a sampling error. The accuracy of TPC in our study was 98.9%, with a sensitivity and specificity of 94.2% (95% CI, 85.8%–98.4%) and 99.7% (95% CI, 98.6%–99.9%), respectively (Fig. 1).


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  		TABLE 2. Results of touch preparation cytology (TPL) and frozen section (FS) of the SLN
 


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  		FIG. 1. Comparison of sensitivity, specificity, and accuracy between touch preparation cytology (TP) and frozen section (FS).

 
Figure 2 demonstrates a three-dimensional cluster of neoplastic cells in a background of a monolayer of lymphocytes. This corresponds to one of our cases of micrometastasis that correlated with a <1-mm micrometastasis found on TPC H&E. Figure 3A is a TPC slide at low power (x100), demonstrating individual neoplastic cells with abundant cytoplasm in the background of small lymphocytes. At a higher power (x400; Fig. 3B), eccentric nuclei with occasional intracytoplasmic vacuoles, histologically associated with lobular carcinoma, can be appreciated. Figure 3C demonstrates the corresponding gross histology of the metastatic lymph node.



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  		FIG. 2. This positive touch preparation slide demonstrates a three-dimensional cluster of neoplastic cells in the background of a monolayer of lymphocytes. Hematoxylin and eosin; original magnification x400.

 


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  		FIG. 3. (A) Touch preparation slide at low power (x100), demonstrating individual neoplastic cells with abundant cytoplasm (thin white line) in the background of small lymphocytes (thick white line). At a higher power (x400) (B), the eccentric nuclei with occasional intracytoplasmic vacuoles (white line), histologically associated with lobular carcinoma, can be appreciated. (C) Corresponding gross histology of the metastatic lymph node on permanent section. Hematoxylin and eosin; original magnification x200.

 
Of the 165 nodes evaluated with FS, 19 showed metastases on permanent H&E. There were 18 nodes positive on FS; 2 (1.4%) were FPs, yielding a positive predictive value of 90.0% (95% CI, 68.3%–98.8%). The FN rate was 15.8%, with a negative predictive value of 97.9% (95 CI, 94.1%–99.6%; Table 2). The accuracy, sensitivity, and specificity were 96.7%, 85.7% (95% CI, 63.6%–96.9%), and 98.6% (95% CI, 95.1%–99.8%), respectively (Fig. 1). On follow-up, to date, there has been no axillary recurrence in the patients who did not receive axillary dissection.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We hope that in this decade SLN biopsy for staging the axilla will become the standard of care in patients with early-stage breast cancer. At our institution the decision to proceed or not proceed with ALND at the initial operation is based on the intraoperative examination of the SLN. Immediate and reliable intraoperative information on the status of the SLN is imperative. The questions to be addressed are what technique is most rapid and accurate in making that decision and how well the intraoperative technique correlates with the final results of permanent pathologic sections, thus preventing a second operation for ALND.

Different techniques (FS, FS plus rapid IHC, and TPC [imprint cytology]) are currently under investigation to address these questions. In reviewing the literature and our own experience, FS is not as sensitive in detecting metastases in SLNs and is more time consuming in comparison to TPC. In addition, a significant amount of tissue is wasted at the time of FS; thus, micrometastases can remain undetected even at the time of evaluation of the permanent section. Weiser et al.20 investigated routine intraoperative FS on SLN. FS was used as the intraoperative technique for evaluation of the SLN in 890 breast cancer patients. Serial sections and IHC staining with cytokeratins were performed on all SLNs that were negative on FS. Their overall results for FS revealed a sensitivity of 58% (135 of 231) and an FN rate of 42% (96 of 231). The benefit of FS in avoiding reoperative ALND ranged from 4% for T1a to 38% for T2 cancers, indicating that the sensitivity of FS increased with tumor size and the presence of macrometastases. Because of the limitation of intraoperative FS to detect micrometastases in small cancers, they concluded that routine FS might not be beneficial in the immediate evaluation of SLNs in such cases.

Veronesi reported a sensitivity of 68% and an FN rate of 32% for intraoperative FS in 81 SLN-positive patients. By use of a more exhaustive technique to improve intraoperative results, Veronesi evaluated the use of intraoperative FS and immediate IHC of the entire SLN (the SLN was frozen in its entirety, 15 or more pairs of 4-µm FSs were stained, and rapid IHC was performed).18 Although the sensitivity (100%) and FN (0%) rates were improved significantly, the intraoperative time required for results ranged from 40 to 50 minutes. The requisite number of pathologists and technologists is unlikely to be available at most institutions. Flett et al.,17 using the FS technique, reported an accuracy of 95% in 53 of 56 patients. Intraoperative results of our FS as compared with permanent serial section H&E showed a sensitivity, specificity, and FN rate of 84.2%, 98.6%, and 15.8%, respectively. The high FN rate was due largely to the failure in detecting micrometastases, consistent with what others have reported.

TPC (imprint cytology) has evolved as a more rapid and accurate technique for the intraoperative evaluation of SLNs. At our institution, results of TPC of SLNs are significantly more sensitive and specific than FS (Fig. 1). The breakdown of T1, T2, and T3 lesions in regard to metastases detected by TPC is listed in Table 3; FN rates were calculated only on positive lymph nodes. The rates of axillary metastases in our study were not different in regard to tumor size and detection of micrometastases in patients with small cancers from those published by most authors.


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  		TABLE 3. Detection of positive sentinel lymph nodes by touch preparation cytology in relationship to tumor size
 
Dudgeon and Patrick23 first reported the use of intraoperative imprint cytology in surgical pathology in 1927. Morris et al.24 used the technique for preoperative lymph node staging for gastric cancer in 25 patients (115 lymph nodes evaluated) and reported a sensitivity of 94% and a specificity of 88%. Since then, numerous investigators have had promising results with this technique, with a reported sensitivity 93% to 100% (Table 4).13–16 Ratanawichitrasin et al.15 prospectively evaluated touch imprint slides from 55 patients with breast cancer. The concordance between TPC and paraffin sections of SLNs was 98% (54 of 55). When TPC of SLNs was compared with permanent sections of all lymph nodes from the ALND, the concordance was 95% (52 of 55), with a reported sensitivity and specificity of 83% and 100%, respectively. The positive and negative predictive values were 100% and 93%, respectively. Quill et al.13 prospectively evaluated lymph node imprint cytology performed on 86 nodes from 13 patients with breast cancer undergoing simple mastectomy with axillary lymph node sampling and showed a diagnostic sensitivity of 93% and a specificity of 98%. In a larger series, Motomura et al.16 evaluated the usefulness of intraoperative imprint cytology (TPC) and FS for SLN in patients with clinically negative axillary lymph nodes. The sensitivity, specificity, and overall accuracy of TPC were 96.0%, 90.8%, and 92.1%, respectively. Of note was that 10 of the SLNs were tumor positive on TPC and tumor negative on initial H&E-stained sections of the permanent section, and micrometastases were found in 8 of the nodes with the addition of IHC. In contrast, van Diest et al.25 reported a sensitivity of 91% for FS and 63% for TPC and concluded that the addition of TPC to FS intraoperatively did improve the results of intraoperative evaluation of the SLN.


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  		TABLE 4. Studies on touch preparation intraoperative evaluation of SLNs
 
Weaver et al.26 reported the results of detailed pathologic analysis of SLNs and non-SLNs from 431 women with breast cancer who were enrolled onto the Vermont multicenter SLN trial. The addition of IHC analysis of the SLN increased the frequency of identifying occult metastases in 10% of women with SLNs found to be free of tumor by conventional methods. van Diest et al.25 reported that IHC increased the percentage of metastases found in lymph nodes from 8% to 41%, with an average of 20%. They found that the gain for detection of IHC micrometastases was highest in patients with lobular carcinoma. In our protocol, IHC was used selectively in patients with suspected micrometastases on permanent H&E and in patients with infiltrating lobular carcinoma, because the single small cell or cluster of cells seen with lobular carcinoma may be mistaken for histocytes on routine staining. Routine use of IHC in SLNs is currently not recommended by the College of American Pathologists as a standard of care in determining node positivity.

In our long-term experience, as well as in our review of the literature, TPC is a fast and accurate technique for intraoperative assessment of the SLN. Although results of FS are acceptable, in comparison, TPC has a higher sensitivity and lower FN rate even in the presence of micrometastases. TPC has the advantages of simplicity and speed, and the entire SLN is conserved without the potential loss of diagnosis, as might be seen with FS. In the end the question is whether there is benefit to the patients. The benefit of TPC is expressed as the proportion of all patients with a positive TPC, which allows an immediate ALND and thus avoids reoperation. TPC provides significant benefit (15.8%) in evaluating the SLN in clinically node-negative breast cancer. TPC (imprint cytology) is the intraoperative technique that we recommend for the evaluation of SLNs.

Received for publication March 18, 2001. Accepted for publication January 18, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  5. Veronesi U, Paganelli G, Viale G, et al. Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst 1999; 91: 368–73.[Abstract/Free Full Text]
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  22. Greenberg RS. Medical Epidemiology. Norwalk, CT: Appleton & Lange, 1993.
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  24. Morris DL, Moore J, Thompson H, Keighley MRB. Preoperative lymph node imprint cytology for staging gastric carcinoma (abstract). Br J Surg 1982; 69: 282.
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