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Nodal Stage Classification for Breast Carcinoma: Improving Interobserver Reproducibility Through Standardized Histologic Criteria and Image-Based Training

Roderick R. Turner, Donald L. Weaver, Gabor Cserni, Susan C. Lester, Karen Hirsch, David A. Elashoff, Patrick L. Fitzgibbons, Giuseppe Viale, Giovanni Mazzarol, Julio A. Ibarra, Stuart J. Schnitt, Armando E. Giuliano

From the John Wayne Cancer Institute at Saint John's Health Center, Santa Monica; David Geffen School of Medicine, University of California at Los Angeles, Los Angeles; St Jude Medical Center, Fullerton; Orange Coast Memorial Medical Center, Fountain Valley, CA; University of Vermont College of Medicine, Burlington, VT; Bacs-Kiskun County Teaching Hospital, Kecskemet, Hungary; Brigham and Women's Hospital; Beth Israel Deaconess Medical Center, Boston, MA; and European Institute of Oncology and University of Milan, Milan, Italy

Corresponding author: Roderick R. Turner, MD, Department of Pathology, Saint John's Health Center, 1328 Twenty-Second St, Santa Monica, CA 90404; e-mail: Roderick.Turner{at}stjohns.org

	ABSTRACT

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Purpose Reliable pathologic stage classification of axillary lymph nodes is an important determinant of prognosis and therapeutic decision making for patients with invasive breast cancer. Pathologists' distinction between micrometastasis (pN1mi) and isolated tumor cells [ITC; pN0(i+)] is variable using the American Joint Committee on Cancer (AJCC) Staging Manual (Sixth Edition). We sought to determine whether a set of clearly defined histologic criteria could lead to reproducible nodal classification by pathologists.

Patients and Methods Digital images of sentinel lymph node biopsies from 56 patients with small-volume nodal metastases were examined by six experienced breast pathologists (MDs), first as a pre-test, and again as a post-test after studying a training program that outlined and illustrated the classification criteria.

Results Post-test results, after study of the training program, were significantly improved. Compared with the reference MD, agreement improved from 76.2% (pre-test = 0.575; standard deviation [SD], 0.25) to 97.3% (post-test = 0.947; SD, 0.049). Multirater analysis of agreement among the six MDs improved from 71.5% (pre-test = 0.487; ASE, 0.039) to 95.7% (post-test = 0.915; ASE, 0.037). Agreement on lobular carcinoma metastasis classification improved from 55% (23 of 42; pre-test) to 100% (42 of 42; post-test) (P < .001), and agreement on ITC classification in nodal parenchyma improved from 67.6% (69 of 102; pre-test) to 98.0% (100 of 102; post-test; P < .001).

Conclusion Application of current definitions for classification of small-volume nodal metastases are inconsistent, leading to variable classification of ITC and micrometastases. Reproducibility of pathologic nodal stage classification is achievable through study of a training set to clarify the AJCC criteria.

	INTRODUCTION

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Reliable pathologic staging of the primary tumor and regional lymph nodes is an essential component of treatment planning for patients with invasive breast carcinoma. Axillary sentinel lymph nodes (SLNs) commonly demonstrate small amounts of metastatic carcinoma¹ that require distinction between micrometastasis (pN1mi) and isolated tumor cells [ITC; pN0(i+)] in the TNM staging system.² This distinction influences individual treatment recommendations and population-based studies of surgical and adjuvant therapies.

Diagnostic variation in the pathologic stage classification of nodal micrometastasis and ITC is recognized as a problem area because American Joint Committee on Cancer (AJCC) guidelines are complex and unclear.^3,4 Practical application has been complicated by the use of different wording in the International Union Against Cancer (UICC) system.⁵ The most challenging issues pertain to measurements of multiple tumor cell clusters or single cells; their microanatomic location in nodal parenchyma, subcapsular sinus, or perinodal tissues; and the dispersed pattern of lobular carcinoma metastases. A clarification of the AJCC Sixth Edition emphasized that the (i+) designation refers to ITC detected by either hematoxylin-eosin (H-E) or cytokeratin immunohistochemistry (IHC), rather than metastases detected exclusively by IHC.⁶ However, clear guidelines on how to measure multiple clusters or single cells have not been provided, which has contributed to the wide variation observed in clinical practice.

Improvements in diagnostic reproducibility have previously been achieved in several areas of breast pathology through the use of standardized histologic criteria. Successful studies have been reported for ductal proliferative lesions,⁷ histologic type⁸ and grade⁹ of carcinoma, and flat epithelial atypia.¹⁰ We hypothesized that a uniform set of histologic criteria and definitions, combined with a well-illustrated training program, could significantly improve interobserver agreement in SLN pathologic stage classification.

	PATIENTS AND METHODS

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Selection of Digital Images
A test set of 56 cases with small amounts of metastatic mammary carcinoma in SLNs was compiled as digital images and placed onto a password-protected Web site at the John Wayne Cancer Institute. Thirty-seven cases were obtained from the Pathology Department files at Saint John's Health Center; 19 cases were utilized from an online site (http://breast-pathology.uni-muenster.de/) of a previously published study⁴ (case numbers 1, 3 to 5, 7, 9, 13, 16, 23, 26, 31 to 33, 35, 37, 39, 43, 45, and 50 in this study). Case selection included both common cases and difficult, challenge cases likely to elicit differences in interpretation, and spanned the spectrum of ITC (single cell to multiple clusters up to 0.2 mm) and micrometastases as single or multiple clusters (0.21 to 2.0 mm). These included a few cases that some observers may interpret as macrometastasis and others that could be interpreted as negative/benign cells only. A calibrated measurement bar was present in each image.

The cases included seven lobular carcinomas (cases17, 23, 30, 41, 42, 51, and 56), 17 metastases with ITC in nodal parenchyma (cases 4, 7, 10, 14, 19, 22, 30, 31, 34, 36, 41, 42, 46, 48, 51, 55, and 56), six metastases very close to the 0.20-mm threshold (cases 8, 24, 25, 31, 39, and 40), and two cases with perinodal metastases (cases 5 and 52). The cases had one (n = 34), two (n = 18) or three (n = 4) images. Twenty-nine cases utilized cytokeratin IHC; the other 27 were H-E stains. Forty-one cases had multiple clusters or single cells.

Participant Pathologists and Study Format
Seven experienced breast pathologists with an interest in SLN pathology were recruited for the study (G.C., P.L.F., J.A.I., S.C.L., G.M., G.V., D.L.W.). Because two pathologists (G.M., G.V.) worked as a team and submitted one answer set, the working group comprised six MDs whose diagnoses were compared with a reference pathologist (R.R.T.) and with each other. A pre-test consisting of 56 cases was conducted in which the six participant pathologists (MDs) applied diagnostic criteria that they utilize in daily practice. Answers were recorded (ITC, Micro, Other) and submitted to the study coordinator (K.H.), who applied a code (MD#) for individual confidentiality.

The same 56 cases were utilized in the post-test after random reordering by the study statistician (D.A.E.). Before the post-test, the MDs were asked to study a training program that included definitions, guidelines, example images, and instructions for classification, then to apply those criteria in the post-test despite any potential disagreement with the criteria. The study coordinator received, tabulated, and submitted the results to the statistician for analysis.

Training Program and Study Criteria
The study criteria were based on the concept that ITC and micrometastases are distinguished by the size of the largest tumor cell cluster, regardless of their microanatomic location within or adjacent to the lymph node, and regardless of the number of clusters or single cells. Specific definitions are shown in Table 1.

	RESULTS

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Pre-Test Results
Agreement between the MDs and the reference pathologist was only moderate in the pre-test, with a group average agreement of 76.2% (range, 57.1 to 96.4, ± 14.8) and a statistic of 0.575 (± 0.25; Table 2). In multirater analysis, the overall percentage of agreement among the six MDs before training was 71.5% (601 of 840), with a multirater of 0.487 (ASE, 0.039). This diagnostic variability was comparable with previously published studies,^3,4 and indicated that the test images would provide a rigorous trial for the study criteria.

View larger version (80K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Lobular carcinoma (test case #17). The dispersed pattern of lobular carcinoma caused diagnostic variation on (A) pre-test (four MDs chose macrometastasis and two MDs chose micrometastasis). On (B) post-test, all six MDs agreed with micrometastasis.

View larger version (80K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Lobular carcinoma (test case #56). A dispersed pattern of lobular carcinoma with fewer cells than the case illustrated in Figure 2 also caused disagreement in classification. On (A) pre-test, three MDs chose micrometastasis, one chose "other", and two chose isolated tumor cells (ITC). On (B) post-test, all six MDs chose ITC [(N0(i+)].

The training program criteria led to significant improvement with classification of lobular carcinoma metastases. Post-test agreement between the six MDs and reference MD was 100% (42 of 42), compared with 55% (23 of 42) in the pre-test (P < .001). The dispersed pattern with multiple single cells and small clusters demonstrated excellent concordance (100%) on post-test (Figs 1 and 2).

The training program criteria led to significant improvement in agreement for ITC in nodal parenchyma (Fig 3). Post-test agreement between the six MDs and reference MD, for ITC in nodal parenchyma (17 cases), was 100 of 102 (98.0%) compared with 69 of 102 (67.6%) pre-test (P < .001).

View larger version (144K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 3. Isolated tumor cells (ITC) in nodal parenchyma and subcapsular sinus (test case #14). Predominantly sinusoidal clusters, but a few cells extended into the lymphoid tissue. On pre-test, this case was classified by three MDs as micrometastasis, and by three MDs as ITC. On post-test, all six MDs chose the ITC category.

Tumor cell clusters very close to the 0.20-mm threshold were identified as a problem area on pre-test and also showed poor reproducibility on post-test. These were unusually difficult, borderline lesions. Six cases (cases 8, 24, 25, 31, 39, and 40) with clusters from 0.18 to 0.23 mm were discordantly classified compared with the reference MD on both pre-test (31%; 11 of 36) and post-test (25%; eight of 36). Case 31 demonstrated a small cluster difficult to visualize on H-E stain (Fig 4A). It was measured by the reference MD as 0.20 mm and considered an ITC cluster. On pre-test, four MDs favored micrometastasis and two MDs chose ITC. On post-test, two MDs chose micrometastasis and four chose ITC. For case 25 (Fig 4B), the reference MD measured the cluster at 0.205 mm, considered it indeterminate or borderline, and chose the lower category, ITC. On pre-test, four MDs classified it as micrometastasis and two chose ITC. On post-test, three MDs chose micrometastasis and three chose ITC.

View larger version (64K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 4. Tumor cell clusters with sizes around the 0.2 mm threshold between isolated tumor cells (ITC) and micrometastasis caused interpretive variation in both pre-test and post-test. The reference MD considered both of these cases to be ITC clusters at the 0.2 mm threshold. (A) Case #31 (hematoxylin and eosin staining, x200); (b) case #25 (immunohistochemistry, x400).

	DISCUSSION

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The six MDs showed excellent agreement in the post-test, both in comparison with the reference MD and in multirater analysis, with significant improvement compared with their pre-test results (Wilcoxon signed rank P < .001). Two of the most problematic areas on pre-test, lobular carcinoma metastases and ITC in nodal parenchyma, also showed outstanding concordance on post-test (P < .001).

The few persistent discordant classifications observed in the post-test occurred almost exclusively with tumor cell clusters of borderline size near the 0.20-mm threshold. Two cases interpreted by the reference MD as ITC had clusters that measured 0.20 mm (case 31) and 0.205 mm (case 25), respectively, and two cases interpreted as micrometastasis had clusters that measured 0.22 mm (case 8) and 0.23 mm (case 39), respectively. A useful guideline in the AJCC system and the current study training program to prevent overstaging of minimal nodal disease is that a pathologist faced with a borderline finding should select the lower category. Further refinements in these proposed criteria may help to achieve better reproducibility with borderline-size metastases. However, no training program would be expected to resolve minor variations in microscopic measurements,¹³ and it would not be expected that practicing pathologists be obligated to measure ITC as precisely as was done for this study.

The concept of benign transport of epithelial cells to axillary lymph nodes, albeit of genuine concern,^14,15 has contributed to diagnostic variation in the pathologic staging of breast cancer. The position taken with this study is that epithelial cells and minute clusters with atypia comparable to the patient's primary invasive carcinoma found in the SLN should be regarded as ITC [pN0(i+)], because histologic features of minimal nodal disease do not permit determination of metastatic potential.^16,17 Cytokeratin-positive debris should be excluded and classified as pN0(i–).

The current study has focused on interpretive issues for small-volume nodal metastases, but it should be noted that there are other causes of diagnostic variability for SLN biopsies, which include differences in intraoperative pathologic techniques, the number and depth of paraffin section levels examined, and the use of cytokeratin IHC or reverse transcriptase polymerase chain reaction methods.^18-23 The widespread use of multiple level sections and IHC in current practice frequently detects small-volume metastases that are of uncertain clinical significance. This study utilized selected digital images to control for all variables except the interpretive component. Actual results in clinical practice with microscopic glass slides may not be quite as good, because the pathologist would first need to detect the small metastases.²⁴

Axillary SLN status, for patients with early-stage invasive breast carcinoma, remains an important determinant of prognosis and a basis for treatment recommendations. At many institutions, patients with negative SLN results, including those with ITC [pN0(i+)], are spared further axillary node dissection or axillary radiation therapy, whereas node-positive patients, including those with micrometastasis (pN1mi), commonly receive further axillary treatment.²⁵ Additionally, the choices for chemotherapy and hormonal therapy may be adjusted on the basis of nodal stage classification. The distinction between ITC and micrometastasis is important in its impact on the total number of positive lymph nodes with respect to categoric nodal classification. Lymph nodes containing ITC only are not included in the decision to classify a breast carcinoma as pN1 (one to three nodes positive), pN2 (four to nine nodes positive), or pN3 ( 10 nodes positive).

Arbitrarily set criteria, such as those used in the current study and the pTNM system,^2,5 do not necessarily provide the best prognostic separation; but, without diagnostic reproducibility, meaningful prognostic separation is not possible. Although excellent agreement can be reached with clearly defined criteria, pathologists, including some in this study, are reluctant to classify a patient's SLN as negative [ie, pN0(i+)] when it contains numerous dispersed single tumor cells with a collective volume that would exceed a few dozen cohesive tumor cells classified as micrometastasis (pN1mi). This situation requires clarification in future staging manuals, while recognizing that reproducibility is a precondition for the clinical utility of a test result.

As proven by our pre-test results and by prior studies^3,4 reproducibility in breast cancer nodal stage classification cannot be achieved solely on the basis of the available AJCC/UICC text definitions. We have provided a method to improve on those definitions by including visual examples for a process that requires interpretation of visual input. Reproducibility of pathologic nodal stage classification is achievable through a set of simple and uniform diagnostic criteria presented in a visual training program and reported in this study. In an era with widespread access to electronic archives, illustrative examples would be a logical extension to the AJCC/UICC staging manual.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author(s) indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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Conception and design: Roderick R. Turner, Susan C. Lester, David A. Elashoff, Stuart J. Schnitt

Financial support: Armando E. Giuliano

Administrative support: Karen Hirsch

Provision of study materials or patients: Roderick R. Turner, Gabor Cserni

Collection and assembly of data: Donald L. Weaver, Gabor Cserni, Susan C. Lester, Karen Hirsch, Patrick L. Fitzgibbons, Giuseppe Viale, Giovanni Mazzarol, Julio A. Ibarra

Data analysis and interpretation: Roderick R. Turner, Gabor Cserni, Susan C. Lester, David A. Elashoff, Armando E. Giuliano

Manuscript writing: Roderick R. Turner, Donald L. Weaver, Gabor Cserni, David A. Elashoff

Final approval of manuscript: Roderick R. Turner, Donald L. Weaver, Gabor Cserni, Susan C. Lester, David A. Elashoff, Patrick L. Fitzgibbons, Giuseppe Viale, Giovanni Mazzarol, Julio A. Ibarra, Stuart J. Schnitt, Armando E. Giuliano

	NOTES

 
Supported by funding from the Ben B. and Joyce E. Eisenberg Foundation (Los Angeles, CA), the Fashion Footwear Association of New York Charitable Foundation (New York, NY), and the Associates for Breast and Prostate Cancer Studies (Santa Monica, CA). Supplemental data are available online at www.jco.org.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

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Submitted June 21, 2007; accepted October 11, 2007.

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