Cellular Dyscohesion in Fine-Needle Aspiration of Breast Carcinoma Prognostic Indicator for Axillary Lymph Node Metastases?

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1 natomic Pathology / PROGNOSTIC INDICTOR FOR XILLRY LYMPH NODE METSTSES Cellular Dyscohesion in Fine-Needle spiration of reast Carcinoma Prognostic Indicator for xillary Lymph Node Metastases? nne. Schiller, MD, Talaat S. Tadros, MD, George G. irdsong, MD, and Norman. Grossl, MD Key Words: Fine-needle aspiration; Cytopathology; reast carcinoma; Cellular dyscohesion bstract The role of fine-needle aspiration (FN) in the diagnosis of breast carcinoma is established. We evaluated whether the degree of cellular dyscohesion and the nuclear grade in FN material of breast carcinomas are reliable prognostic predictors for ipsilateral axillary lymph node metastasis. FN specimens from 98 women with infiltrating ductal and infiltrating lobular carcinomas were evaluated by 2 observers for degree of cellular dyscohesion and nuclear grade. Follow-up specimens from lumpectomy and/or mastectomy with axillary dissection were available for each patient. y univariate analysis, degree of cellular dyscohesion and nuclear grade were not predictive of axillary lymph node metastasis regardless of tumor size. High histologic grade, size greater than 2 cm, and patient age younger than 52 years were significant predictors of metastasis. y multivariate analysis, size greater than 2 cm and age younger than 52 years were statistically significant for lymph node metastasis. In contrast with a published study, the results of the present study fail to show cellular dyscohesion in FN specimens as predictive of lymph node metastasis; however, the scoring method for determining the degree of cellular dyscohesion is reproducible between 2 independent observers. Fine-needle aspiration (FN) is used widely in the initial management of breast lesions. 1 This technique, which is safe, simple, and inexpensive, can accurately diagnose carcinoma. During the past decades, FN of the breast has reduced the need for open surgical biopsy with its higher cost to the health care system and potentially greater morbidity. In addition, material procured from FN of malignant breast tumors can be evaluated by ancillary studies for prognostic factors, including estrogen and progesterone receptor status, 2,3 DN ploidy, 4 and HER2/neu expression. 5 Cellular dyscohesion is a secondary diagnostic feature that, in combination with malignant cytologic criteria, is helpful in the diagnosis of malignant neoplasms. Cytologic smears of breast carcinomas obtained by FN display varying degrees of dyscohesion with small clusters of cells and single cells. In contrast, benign ductal epithelium with intact cell membranes displays sheets of intact cohesive cells. Cell-to-cell adhesion is influenced by the loss of expression of cell adhesion molecules such as E-cadherin. 6,7 It has been suggested that the degree of cellular dyscohesion, being an inherent feature of aspiration material in FN specimens from malignant breast tumors, may be an independent prognostic indicator for recurrence and regional metastasis One study concluded that the degree of cellular dyscohesion in aspiration material from breast carcinomas smaller than 3 cm is a significant prognostic indicator for axillary metastases. 10 We report our experience from Grady Memorial Hospital, tlanta, G, in a retrospective study that addressed the relationship between cellular dyscohesion in FN specimens of infiltrating breast carcinomas and ipsilateral axillary metastasis. It also evaluated the reproducibility of a scoring system for cellular dyscohesion. m J Clin Pathol 2001;115:

2 Schiller et al / PROGNOSTIC INDICTOR FOR XILLRY LYMPH NODE METSTSES Material and Methods Cases of infiltrating ductal and lobular carcinomas were identified by computer search in the Department of Pathology at Grady Memorial Hospital between January 1993 and December Cases included were all women who underwent preoperative FN of a malignant tumor followed by lumpectomy or mastectomy with an ipsilateral axillary dissection. Ninety-eight women with archival material available for review and who met the aforementioned criteria were identified. Patients with palpable breast masses underwent pathologist-performed breast FNs in the FN clinics at Grady Memorial Hospital. For patients with nonpalpable masses, FNs were performed under ultrasound guidance by radiologists; cytologic smears were prepared immediately and adequacy evaluated by pathologists. FNs were performed using 22- to 25-gauge needles. Cytologic smears were immediately alcohol fixed and then stained with Papanicolaou stain. Other glass slides from the same cases were air dried and then stained with a modified rapid Romanowsky stain. ll FN specimens included in the study were diagnosed as ductal or lobular carcinoma based on cytologic criteria before surgical treatment. Clinical information, the type of procedure, size of mass, type of carcinoma, histologic grade, and lymph node status were obtained from surgical pathology reports. Metastatic carcinoma identified, regardless of number of axillary lymph nodes involved, was recorded as positive. If no metastatic carcinoma was identified, the lymph node status was negative. The histologic grade was determined by using a modified loom and Richardson method. 11 ll FN slides were reviewed independently by 2 experienced cytopathologists (T.S.T. and N..G.). dyscohesion score (DS) was assigned based on proposed criteria. 10 DS of 1 represented cases in which fewer than 25% of the malignant cells were single or loosely cohesive Image 1. DS of 2 was assigned to cases in which 25% to 75% of malignant cells were single or loosely cohesive Image 2. Cases in which more than 75% of malignant cells occurred as single cells or in loosely cohesive groups were given a DS of 3 Image 3. The DS in each case was based on the overall assessment of dyscohesion from all slides available for review and not on the highest degree seen focally or on one slide. The scores then were compared between the 2 pathologists. When 2 scores were discordant, a final consensus DS was assigned after reviewing cases together. The DS was assessed without knowledge of the corresponding histologic diagnosis and lymph node status. In addition to a DS, the FN specimens were evaluated for nuclear grade (NG) of malignant cells by the same cytopathologists. NG was assessed by using criteria proposed by Dabbs and Silverman. 12 Nuclear features that resembled normal ductal epithelium with minimal enlargement, round and smooth nuclear membranes, uniform fine chromatin, and no nucleoli were classified as NG1. Malignant nuclei with moderate anisonucleosis, smooth nuclear membranes, and uniform chromatin with or without small nucleoli were classified as NG2. Malignant cells with marked anisonucleosis with at least a 3-fold variation in diameter, marked hyperchromasia, irregular nuclear membranes, and macronucleoli with or without nuclear clearing were classified as NG3. The highest NG seen was recorded as the NG for individual cases. The NGs were assessed independently. In cases in which discordant NGs existed, the 2 pathologists reviewed the cases together and agreed on a final NG. s Image 1 Fine-needle aspiration specimen of infiltrating ductal carcinoma., Dyscohesion score (DS) of 1 (Papanicolaou, 100)., Same case, with DS of 1 (Papanicolaou, 400). 220 m J Clin Pathol 2001;115:

3 natomic Pathology / ORIGINL RTICLE Image 2 Fine-needle aspiration specimen of infiltrating ductal carcinoma., Dyscohesion score (DS) of 2 (Papanicolaou, 100)., Same case, with DS of 2 (Papanicolaou, 400). with the DS, the NG was assessed without knowledge of the corresponding histologic specimen. The final values of the DS and NG, which were determined independently or by consensus in cases of disagreement, were used in statistical testing using multivariate and univariate analysis. Results The 98 women in the study ranged in age from 27 to 78 years (mean, 52 years). Ninety-three had infiltrating ductal carcinoma, and 5 patients had infiltrating lobular carcinoma diagnosed from surgical material. The FN material from all cases was diagnosed as malignant. The tumor size ranged from 0.5 to 12 cm (mean, 3.1 cm). Forty-eight patients (49%) had metastatic carcinoma in ipsilateral axillary lymph nodes, and 50 patients (51%) had no evidence of metastatic disease. Table 1 gives the DSs and NGs with respect to tumor size and lymph node status. y univariate analysis, neither the DS (P =.491) nor the NG (P =.284) were predictive of axillary lymph node metastasis, regardless of tumor size. High histologic grade (grade 3) of the surgical specimen (P =.007), size greater than 2.0 Image 3 Fine-needle aspiration specimen of infiltrating ductal carcinoma., Dyscohesion score (DS) of 3 (Papanicolaou, 100)., Same case, with DS of 3 (Papanicolaou, 400). m J Clin Pathol 2001;115:

4 Schiller et al / PROGNOSTIC INDICTOR FOR XILLRY LYMPH NODE METSTSES Table 1 Dyscohesion Scores and Nuclear Grades ccording to Tumor Size and Lymph Node Status Dyscohesion Score Nuclear Grade Tumor Size (cm) Lymph Node Status Less than 1 Negative Positive to <2 Negative Positive to <3 Negative Positive or more Negative Positive cm (P =.001), and patient age younger than 52 years (P =.007) were significant predictors of ipsilateral axillary lymph node metastasis. y multivariate analysis, size greater than 2.0 cm (P =.002) and patient age younger than 52 years (P =.023) were statistically significant for the presence of axillary metastases Table 2. In 68 cases (69%), there was complete agreement in the DS between the reviewing cytopathologists. In 30 cases of discordant DSs, the score differed by a score of 1; in no case did the score differ by a score of 2. In 74 cases (76%), there was complete agreement in the NG between the reviewing cytopathologists. In 23 cases of discordant NG, the score differed by a score of 1; in 1 case the score differed by a score of 2. In cases of disagreement, the final consensus DS and NG were agreed on between the reviewers. greement between the reviewers (N..G. and T.S.T.) for independent determination of DS (P =.013) and NG (P =.012), evaluated by kappa (0.46 and 0.52, respectively), was statistically significant. Discussion The present study found histologic grade to be a significant predictor (P =.007) of axillary lymph node metastasis; however, cytologic evaluation of NG was not (P =.284). These findings are similar to those of Yu et al, 10 who found no significant association between NG and metastasis. In 1 case, the NG differed by 2. Further review of that case revealed that Table 2 Predictors of Lymph Node Metastasis Variable Univariate P Multivariate P Dyscohesion score.491 Nuclear grade.284 Histologic grade.007 Size 0-2 vs >2 cm Size vs >2.5 cm.004 ge 52 y vs <52 y the malignant cells displayed a spectrum of NGs, with focal NG 3 present, which was taken as the final score. The present study found no association between the level of cellular dyscohesion on FN material from breast carcinomas and ipsilateral axillary metastasis, regardless of the size of the primary tumor. This finding is in contrast with that of Yu et al, 10 who found the degree of cellular dyscohesion to be prognostically significant for breast carcinomas 3 cm or smaller. In that subgroup, Yu et al 10 identified 4 cases with a DS of 3, all of which metastasized (100%). In contrast, we identified 19 cases smaller than 3 cm with a DS of 3. Thirteen of those 19 cases that were smaller than 3 cm did not metastasize to axillary nodes, the other 6 did (32%). We agree with Yu et al 10 in that there was no statistically significant association between DS and axillary metastasis in carcinomas larger than 3 cm and the evaluation of greater numbers of breast tumors and neoplasms of other organ systems is warranted. The same criteria to evaluate DSs and NG were used in the present study as in the study by Yu et al. 10 Differences between the present study and that by Yu et al 10 are that more patients were included (98 vs 83) and that 2 cytopathologists independently evaluated slides for DS and NG instead of 1. It is unclear whether the DS in the study by Yu et al 10 was determined from an overall assessment from all slides in a case or from the highest degree of cellular dyscohesion on 1 slide or focally. We have found that the highest degree of cellular dyscohesion can differ in areas within the same slide and between slides. In particular, the cellular dyscohesion often was greater at the edge of smeared material compared with areas away from the edges. This is significant since dyscohesion of cells at the edge of smeared material may have a DS of 3 focally but an overall DS of 2 from all slides and areas. There is an initial learning curve when assigning a DS to a case, since this grading system is qualitative and somewhat subjective, yet it is easily learned. We found that the DSs and NGs used by Yu et al 10 are reproducible. The relationship between cells can be altered 222 m J Clin Pathol 2001;115:

5 natomic Pathology / ORIGINL RTICLE by the pressure applied in preparing glass slides of aspirated material. The number of single cells in a smear may vary with the amount of mechanical pressure used in making the smear. Such mechanical differences may be a source of variability of the DS between smear makers. further limitation of using cellular dyscohesion as a possible prognostic indicator is in aspiration of ductal carcinoma in situ (DCIS) lesions. DCIS may present as a discrete mass amenable to FN. y definition, DCIS does not bridge basement membranes, enter lymphatic vessels, and metastasize to axillary lymph nodes. Yet, high-grade DCIS, in particular the comedo subtype, can display a high degree of cellular dyscohesion in aspiration smears, with a DS of 3 (personal observation, N..G.). lthough there are reported cytologic features that may differentiate infiltrating carcinoma from DCIS in FN material, the consensus is that DCIS and infiltrating carcinoma cannot often be differentiated easily in aspiration material In the light of the findings in the present study and the high degree of dyscohesion seen in cases of high-grade DCIS, we do not believe cellular dyscohesion is a reliable prognostic indicator of axillary metastasis. 8. Stenkvist, engtsson E, Eriksson O, et al. morphometric expression of differentiation in fine-needle biopsies of breast cancer. Cytometry. 1981;1: Layfield LJ, Robert ME, Cramer H, et al. spiration biopsy smear pattern as a predictor of biologic behavior in adenocarcinoma of the breast. cta Cytol. 1992;36: Yu GH, Cajulis RS, DeFrias DVS. Tumor cell (dys)cohesion as a prognostic factor in aspirate smears of breast carcinomas. m J Clin Pathol. 1998;109: loom HJG, Richardson WW. Histologic grading and prognosis in breast cancer: a study of 1409 cases of which 359 have been followed for 15 years. r J Cancer. 1957;11: Dabbs DJ, Silverman JF. Prognostic factors from the fineneedle aspirate: breast carcinoma nuclear grade. Diagn Cytopathol. 1994;10: Wang HH, Ducatman S, Eick D. Comparative features of ductal carcinoma in situ and infiltrating ductal carcinoma of the breast on fine-needle aspiration biopsy. m J Clin Pathol. 1989;92: Sneige N, White V, Katz RL, et al. Ductal carcinoma-in-situ of the breast: fine needle aspiration cytology of 12 cases. Diagn Cytopathol. 1989;5: Theocharous C, Greenberg ML. Cytologic features of ductal carcinoma in situ. Diagn Cytopathol. 1996;15: From the Departments of Pathology, Emory University School of Medicine and Grady Memorial Hospital, tlanta, G. Nominal financial support provided by the Department of Pathology, Emory University. ddress reprint requests to Dr irdsong: Dept of natomic Pathology, Grady Memorial Hospital, 80 utler St, tlanta, G References 1. Costa MJ, Tadros T, Hilton G, et al. reast fine needle aspiration cytology: utility as a screening tool for clinically palpable lesions. cta Cytol. 1993;37: Masood S. Estrogen and progesterone receptors in cytology: a comprehensive review. Diagn Cytopathol. 1992;8: Masood S. Prognostic and diagnostic implications of estrogen and progesterone receptor assays in cytology. Diagn Cytopathol. 1994;10: Lajoie G, Zbieranowski I, Demianiuk C, et al. comparative study of DN quantitation in breast carcinoma with image cytometric analysis and in vitro fine-needle aspiration with flow cytometric analysis. m J Clin Pathol. 1993;100: Corkill ME, Katz R. Immunocytochemical staining of c-erb -2 oncogene in fine-needle aspirates of breast carcinoma: a comparison with tissue sections and other breast cancer prognostic factors. Diagn Cytopathol. 1994;11: Oka H, Shiozaki H, Kobayashi K, et al. Expression of E- cadherin cell adhesion molecules in human breast cancer tissues and its relationship to metastasis. Cancer Res. 1993;53: irchmeier W, ehrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. iochim iophys cta. 1994;1198: m J Clin Pathol 2001;115:

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