Comparative Features of Ductal Carcinoma In Situ and Infiltrating Ductal Carcinoma of the Breast on Fine-Needle Aspiration Biopsy

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1 Comparative Features of In Situ and of the Breast on Fine-Needle Aspiration Biopsy HELEN H. WANG, M.D., DR. P.H., BARBARA S. DUCATMAN, M.D., AND DAWN EICK, CT(ASCP) To evaluate the usefulness of fine-needle aspiration biopsy of the breast in separating ductal carcinoma in situ (DCIS) from infiltrating ductal carcinoma, the authors reviewed 16 preoperative fine-needle aspiration biopsies from biopsy-proven exclusive DCIS and 39 fine-needle aspiration biopsies from infiltrating ductal carcinomas with or without an in situ component. Seven (44%) of the DCIS and eight (21%) of the infiltrating ductal carcinomas had inadequate material for diagnosis on the aspiration biopsy. Five (32%) of the DCIS and 29 (74%) of the infiltrating ductal carcinomas caused suspicion or had positive results for malignancy. Four (25%) of the DCIS and two (5%) of the infiltrating ductal carcinomas showed atypical cells. Morphologic features of the atypical or malignant cells in the adequate specimens from these two lesions were similar except that the cells from the infiltrating ductal carcinomas showed more irregular nuclear spacing (94% vs. 44%, P < 0.01) and more pronounced nuclear overlapping (65% vs. 33%) than those from the DCIS. In addition, the fine-needle aspiration biopsies of the DCIS tended to be hypocellular (< 10 cells/lox) (44% vs. 6.5%, P < 0.05) and to contain benign epithelial cells (22% vs. 6.5%) and macrophages (33% vs. 13%). Although the suspicion of DCIS might be raised when hypocellularity, benign epithelial cells, and macrophages are noted in afine-needleaspiration biopsy of the breast that has positive results or causes suspicion for malignancy,fine-needleaspiration biopsy cannot be relied upon to distinguish DOS from infiltrating ductal carcinoma. (Key words: fine-needle aspiration biopsy; Breast; carcinoma in situ; ductal carcinoma.) Am J Clin Pathol 1989;92: FINE-NEEDLE ASPIRATION BIOPSY (FNAB) of the breast has been used increasingly to triage patients with either palpable breast masses or suspicious mammograms for further management." 1517 Although FNAB of breast has been proved to be an accurate diagnostic tool for breast cancers," 13 its ability to distinguish ductal carcinoma in situ (DCIS) from infiltrating ductal carcinoma has not been adequately investigated. Because patients with exclusive DCIS have different treatment options than those with infiltrating carcinoma, 14 it is important to identify such patients before the definitive treatment plan is made and carried out. We, therefore, undertook the study to Received January 25, 1989; received revised manuscript and accepted for publication April 26, Address reprint requests to Dr. Wang: Department of Pathology, Beth Israel Hospital, 330 Brookline Avenue, Boston, Massachusetts Departments of Pathology, Beth Israel Hospital and Harvard Medical School, Boston, Massachusetts determine if FNAB can be useful in separating patients with exclusive DCIS from those with infiltrating ductal carcinoma. Materials and Methods All patients who had biopsy-proven exclusive DCIS at the Pathology Department of Beth Israel Hospital, Boston, during a 15-month period (January 1, 1987 to March 31, 1988) and had FNAB of the breast before the surgery were included in the study. The performers of these FNABs were identified. All patients who had biopsyproven infiltrating ductal carcinoma with or without an in situ component and preoperative FNAB performed by the previously identified operators during the same 15- month period were included as the comparison group. All aspirates were preserved in 50% ethanol and centrifuged at 5,000 rpm for 5 minutes. The supernatant was discarded, and the pellet was overlaid with Saccomanno's fixative. Cytocentrifuge slides were made on a Shandon cytocentrifuge at 1,400 rpm for 5 minutes. All slides were stained with Papanicolaou's stain. Slides were reviewed for the quantity of atypical epithelial cells (none, a total of 10 or fewer cells, an average of 2-10 cells per 10X, cells per 10X, cells per 10X, or more than 100 cells per 10X); cell groupings (flat sheets, tight three-dimensional clusters, or loosely cohesive clusters); presence of single atypical epithelial cells (none, fewer than 10% of all the atypical epithelial cells, 10-50% of all the atypical epithelial cells, or more than 50% of all the atypical epithelial cells); and background (clean, cystic with proteinaceous material and macrophages, dirty with tumor diathesis, inflammatory, or bloody). A specimen was considered to be inadequate for diagnosis when fewer than ten epithelial cells were present. Cytologic features of the atypical epithelial cells evaluated included the size of nuclei (normal vs. enlarged); nucleus to cytoplasm ratio (normal vs. increased); chromatin pattern (finely granular, coarsely granular, or clear); presence of hyperchromasia; 736

2 Vol. 92 No. 6 FINE-NEEDLE ASPIRATION OF THE BREAST 737 Table 1. Mean Age and Lesion Characteristics of Patients In Situ Total number of patients Mean age of patients (years) Number of palpable lesions (%) 5 (31) 22 (56) Table 3. Cytologic Diagnoses of s by Method of Detection Cytologic Diagnoses Nonpalpable* Palpable Total Inadequate material 6(35%) 2(9%) 8(21%) Atypical 1 (6%) 1 (5%) 2 (5%) Suspicious 4(24%) 3(14%) 7(18%) Positive 6(35%) 16(73%) 22(56%) Total 17(100%) 22(101%) 39 (100%) * Specimens were obtained under the guidance of standard mammography. presence as well as size and number of nucleoli; and presence of pleomorphism, nuclear overlap, nuclear spacing, dyscohesion, and distinct cell borders. Two cytopathologists (H.H.W. and B.S.D.) first reviewed all the slides independently. The discrepancies were reexamined and resolved by consensus. The nature of the lesion was also recorded: palpable masses versus nonpalpable suspicious lesions on mammograms. Aspiration specimens from the latter group were obtained with the guidance of standard mammography for needle localization. 10 Statistical significance for comparison was determined by Fisher's exact test. Results Sixteen patients who had biopsy-proven exclusive DCIS during the study period had preoperative FNAB of the breast. These were performed by four different clinicians. During the same time period, 39 of the patients who had FNAB done by these four clinicians had infiltrating ductal carcinoma on breast biopsy or mastectomy specimen. The mean age of the 16 women with DCIS was 58 years, which was virtually the same as the mean age of 57 for the 39 women with infiltrating carcinoma (with or without an in situ component) (Table 1). Although not statistically significant, fewer patients with DCIS presented with a palpable mass than those with infiltrating carcinoma (31% vs. 56%, P > 0.05). A higher percentage of the FNABs from the in situ carcinomas were inadequate for diagnosis than those from the infiltrating carcinomas (44% vs. 21%, P> 0.05) (Tables 2 and 3), and a lower percentage of the FNABs from the in situ carcinomas were suspicious or positive for carcinoma than those from the infiltrating carcinomas (32% vs. 74%, P < 0.01). Although the nonpalpable infiltrating carcinomas tended to yield inadequate material when compared with the palpable ones (35% vs. 9%, P > 0.05), this was not true for the in situ carcinomas (36% vs. 60%). Interestingly, the nonpalpable in situ carcinomas and the nonpalpable infiltrating carcinomas had virtually the same rate of inadequate material on FNAB (36% vs. 35%). Table 4 shows a comparison of the features of adequate FNAB from the DCIS and the infiltrating ductal carcinomas. The aspiration specimens from the in situ carcinomas were more likely to be hypocellular (P < 0.05) and to contain benign epithelial cells (Fig. 1) and macrophages, and less likely to contain fibroadipose tissue. Only the difference in cellularity is statistically significant. Table 5 shows a comparison of the cytologic features of FNAB from the DCIS and the infiltrating carcinomas. Most of the examined features were present in similar percentages of cases of these two categories of carcinoma. carcinoma tended to show irregular nuclear spacing (P < 0.01) and pronounced nuclear overlapping in a higher percentage of cases than the DCIS. It should be noted that our observations were based on cytocentrifuge specimens. Although the overall results with this preparation are not significantly different from Table 4. Comparison of General Features Between the In Situ and the Table 2. Cytologic Diagnoses of s In Situ by Method of Detection Features In Situ (%) (%) Cytologic Diagnosis Nonpalpable* Palpable Total Inadequate material 4 (36%) 3 (60%) 7 (44%) Atypical 3 (27%) 1 (20%) 4 (25%) Suspicious 2(18%) 0 2(13%) Positive 2(18%) 1(20%) 3(19%) Total 11(99%) 5(100%) 16(101%) Hypocellularity (2-10 cells/1 OX)* 3-dimensional clusters Single cells (> 10% of atypical cells present) Benign epithelial cells Stromal cells Fibroadipose tissue Macrophages 6/9 (67%) 2/9 (22%) 0/9 (0%) 3/9 (33%) 2/31 (6.5%) 23/31 (74%) 20/31 (65%) 2/31 (6.5%) 18/31 (58%) 8/31 (26%) 4/31 (13%) * Specimens were obtained under the guidance of standard mammography. * The difference is statistically significant with P < 0.05 by Fisher exact test.

3 738 WANG, DUCATMAN, AND EICK f A.J.C.P. December 1989 m FlG. 1 (left). Both benign ductal cells (upper) and malignant epithelial cells (lower) are present in a specimen from a breast with an infiltrating carcinoma and significant ductal carcinoma in situ. Papanicolaou (X400). FIG. 2 (right). Bipolar stromal cells (arrows) are present in a background of malignant epithelial cells and inflammatory cells in a specimen from a breast with infiltrating ductal carcinoma. Papanicolaou (X400). those with the conventional smears,5 the number of cells per field and the morphologic characteristics of cell aggregates may differ. Table 5. Comparison of Cytologic Features Between the In Situ and the In Situ (%) Enlarged nuclei Increased N/C ratio Coarsely granular chromatin Hyperchromasia Large nucleoli Pleomorphism Pronounced nuclear overlapping Irregular nuclear spacing* Dyscohesion Distinct cell border 2/9 (22%) 1/9(11%) 9/9(100%) 3/9 (33%) 8/9 (89%) 0/9 (0%) (%) 16/31 24/31 1/31 16/31 3/31 28/31 20/31 29/31 28/31 0/31 (52%) (77%) (3.2%) (52%) (9.7%) (90%) (65%) (94%) (90%) (0%) * The difference is statistically significant with P < 0.01 by Fisher exact test. Discussion Women with breast cancer can now choose between mastectomy and lumpectomy with radiation as the definitive treatment of their cancer. Consequently, one-stage mastectomy immediately after frozen section of the tumor is less often scheduled. Instead, a tissue diagnosis of malignancy is usually obtained first. The advantages and disadvantages of both treatment plans are presented to the patient, who then decides on a definitive treatment. FNAB of the breast, being easy to perform, minimally invasive, and accurate, appears to be an ideal diagnostic test to document malignancy."15'17 Although FNAB is both sensitive and specific in identifying carcinoma in the breast,2'1''14'15 its ability to distinguish between an exclusive DCIS and an invasive tumor has not been adequately investigated. Because there is no recognized standard treatment for exclusive DCIS and it is still controversial whether axillary sampling is indicated in such a lesion,14 it is important to identify these lesions before the definitive treatment in order to explore therapeutic options. The

4 Vol. 92 No. 6 FINE-NEEDLE ASPIRATION OF THE BREAST 739 distinction between an exclusive DCIS and an infiltrating carcinoma becomes even more important when interpreting mammographically directed FNAB from nonpalpable breast lesions, because 13-34% of the malignancies identified in such lesions are DCIS. 310 carcinoma in situ cannot be differentiated from infiltrating carcinoma by physical examination. In our study, 31% of the DCIS presented with a palpable mass, and 69% were detected because of mammograms that caused suspicion (Table 1), a figure similar to the 59% reported in the literature.' The presence of a mass definitely cannot serve as a distinguishing feature between in situ and infiltrating carcinomas. Mammographic features are not particularly helpful in this regard either. 4 ' 9 Although microcalcifications that cause suspicion are more likely to be DCIS than are mass lesions that cause suspicion, sufficient overlap exists that they cannot be relied on to separate these two types of breast carcinoma. Based on a study of FNAB of the breast from ten cases of infiltrating ductal carcinoma and two cases of DCIS, Dziura and Bonfiglio concluded that none of the features they studied were capable of distinguishing DCIS from infiltrating carcinomas. 6 A study of nuclear DNA content of breast carcinomas also suggested that the invasive and noninvasive components of the same tumor cannot be distinguished by DNA analysis. 7 Our results show that the DCIS and the infiltrating carcinoma cannot be distinguished based on the morphologic characteristics of the malignant cells. Nonetheless, a few differences appear to be present between the FNAB of an exclusive DCIS and that of an infiltrating ductal carcinoma. The cytologic features of these tumors conceivably vary according to their subtypes. Because of the small number of cases involved, it is not possible to make meaningful comparisons between different subtypes of tumors. The comparison is made instead between all cases of DCIS and all cases of infiltrating ductal carcinoma in our study. The aspiration specimens from our cases of exclusive DCIS tend to render inadequate material for diagnosis more frequently (Tables 2 and 3). This cannot be explained by the fact that 69% of the in situ carcinomas are nonpalpable, because the palpable in situ carcinomas in our series yielded a higher, though not statistically significantly so, percentage of inadequate specimens than the nonpalpable ones (60% vs. 36%) (Table 3). This finding may suggest that mammography is a better method to localize DCIS than palpation. The higher rate of inadequate material on FNAB from DCIS may result from the fact that the DCIS tends to render hypocellular specimens (Table 4). Even among the adequate specimens, 56% of FNABs from the in situ carcinomas were hypocellular, with only two to ten cells per 10X field. In contrast, less than 10% of the adequate specimens from the infiltrating carcinomas were hypocellular (P < 0.05). This may result, in part, from the smaller average number of malignant cells contained in unit volume of breast tissue with in situ carcinoma than that with infiltrating carcinoma. Although exclusive DCIS tends to yield a hypocellular specimen, the reverse is not true. The reasons for an inadequate or hypocellular specimen are many, such as the lack of skill on the part of the performer, 2 the small size of the tumor, 2,8 and prominent fibrosis of the lesion. 12 Hypocellularity may suggest an in situ lesion, but it is by no means diagnostic. The specimens from DCIS are more likely to have benign epithelial cells and macrophages. DCIS is often present right in the midst of fibrocystic changes. The benign elements from adjacent fibrocystic changes could conceivably be withdrawn simultaneously with malignant ones. In fact, the two cases of the infiltrating carcinomas that contained benign epithelial cells in the FNAB showed extensive DCIS on histologic examination of the lesion. It is very likely that the needle went through the in situ component and withdrew benign elements from the adjacent fibrocystic changes. Similarly, among the four cases of infiltrating carcinoma that had macrophages in the FNAB, two showed extensive DCIS and the other two focal DCIS on histologic examination. Although stromal cells are usually reported to be seen in FNAB from benign lesions, 316 we found bipolar stromal cells in 56% of the FNABs from the DCIS cases and in 58% of the FNABs from the infiltrating carcinomas. The stromal cells we noticed in these specimens are not the oval stripped nuclei often observed in association with fibroadenomas. Instead, they are spindle-shaped, bipolar cells (see Fig. 2). We believe that in the case of infiltrating carcinomas, they probably represent stromal cells from tumor stroma. We also believe that tumor infiltration into fibroadipose stroma "breaking it up" and making it easier to withdraw may explain the finding of fibroadipose fragments being present in 26% of the specimens from the infiltrating carcinomas but in none of the exclusive DCIS. In summary, based on our limited experience of 9 cases of DCIS and 31 cases of infiltrating ductal carcinoma, we do not believe that we can distinguish exclusive DCIS from infiltrating carcinoma on FNAB of the breast. This may become a particularly important pitfall when interpreting FNAB of nonpalpable breast lesions obtained with mammographic guidance, because a considerable percentage of these lesions are DCIS. Nonetheless, we found a few features on FNAB that may suggest an exclusive DCIS. To alert the clinician that the lesion may be an exclusive DCIS and may require further evaluation before definitive treatment, we have been reporting the result of FNAB of breast as positive or suspect for "carcinoma, cannot exclude only an in situ carcinoma" when we noticed hypocellularity or concomitant benign epithelial cells and macrophages in a specimen that contains groups of

5 740 WANG, DUCATMAN, AND EICK A.J.C.P. December 1989 obviously malignant or highly suspect cells. Our results, although inconclusive, suggest that further evaluation of these features in a prospective study of a much larger series is needed. Acknowledgment. The authors thank Peter K. Gardner for excellent secretarial assistance. References 1. Baker LH. Breast Cancer Detection Demonstration Project: fiveyear summary report. CA 1982;32: Barrows GH, Anderson TJ, Lamb JL, Dixon JM. Fine-needle aspiration of breast cancer. Cancer 1986;58: Bibbo M, Scheiber M, Cajulis R, Keebler CM, Wied GL, Dowlatshahi K. Stereotaxicfine-needleaspiration cytology of clinically occult malignant and premalignant breast lesions. Acta Cytol 1988;32: Ciatto S, Cataliotti L, Distante V. Nonpalpable lesions detected with mammography: review of 512 consecutive cases. Radiology 1987;165: Dundas SAC, Sanderson PR, Matta H, Shorthouse AJ. Fine needle aspiration of palpable breast lesions. Results obtained with cytocentrifuge preparation of aspirates. Acta Cytol 1988;32: Dziura BR, Bonfiglio TA. Needle cytology of the breast: a quantitative and qualitative study of the cells of benign and malignant ductal neoplasia. Acta Cytol 1979;23: Erhardt K, Auer GU. Mammary carcinoma. Comparison of nuclear DNA content from in situ and infiltrative components. Anal Quant Cytol Histol 1987;9: Frable WJ. Needle aspiration of the breast. Cancer 1984;53: Hall FM, Storella JM, Silverstone DZ, Wyshak G. Nonpalpable breast lesions: recommendations for biopsy based on suspicion of carcinoma at mammography. Radiology 1988;167: Hann L, Ducatman BS, Wang HH, Fein V, Mclntire JM. Nonpalpable breast lesions: evaluation by fine needle aspiration cytology. Radiology 1989;171: Hermansen C, Poulsen HS, Jensen J, et al. Diagnostic reliability of combined physical examination, mammography, andfineneedle puncture ("triple-test") in breast tumors. Cancer 1987;60: Kreuzer G, Zajicek J. Cytologic diagnosis of mammary tumors from aspiration biopsy smears. III. Studies on 200 carcinomas with false negative or doubtful cytologic reports. Acta Cytol 1972; 16: Palombini L, Fulciniti F, Vetrani A, et al. Fine-needle aspiration biopsies of breast masses. Cancer 1988;61: Schnitt SJ, Silen W, Sadowsky NL, Connolly JL, Harris JR. carcinoma in situ (intraductal carcinoma) of the breast. N Engl J Med 1988;318: Silverman JF, Lannin DR, O'Brien K, Norris HT. The triage role of fine needle aspiration biopsy of palpable breast masses. Diagnostic accuracy and cost-effectiveness. Acta Cytol 1987,31: Vilaplana EV, Jimenez-Ayala M. The cytologic diagnosis of breast lesions. Acta Cytol 1975;19: Wanebo HJ, Feldman PS, Wilhelm MC, Covell JL, Binns RL. Fine needle aspiration cytology in lieu of open biopsy in management of primary breast cancer. Ann Surg 1984;199:

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