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1
Department of Diagnostic Radiology, Yale University School of Medicine, 333
Cedar St., New Haven, CT 06520.
2
Department of Pathology, Yale University School of Medicine, New Haven, CT
06520.
Received January 20, 2000;
accepted after revision March 16, 2000.
Presented at the annual meeting of the American Roentgen Ray Society, New
Orleans, May 1999.
Abstract
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MATERIALS AND METHODS. Retrospective review of 11-gauge vacuum suction biopsy was performed to identify lesions diagnosed as atypical ductal hyperplasia or carcinoma. The histology of the core and surgical specimens was compared. Of 158 cases of cancer, underestimation occurred in 15 (9.5%). The mammographic and histologic features were assessed.
RESULTS. Of 15 underestimated cases, six were atypical ductal hyperplasia that proved to be cancer (5 ductal carcinoma in situ and 1 invasive) and nine were ductal carcinoma in situ that proved to have invasion. The underestimation rate for calcifications was 16.3% (14/86) and for masses was 1.6% (1/64) (p = 0.007). Most (5/6) underestimated atypical ductal hyperplasia cases were reported as "markedly atypical," and four of nine underestimated ductal carcinoma in situ cases were reported as "possible invasion." No significant difference was seen in the number of core specimens obtained or the sizes of the lesions for underestimated cases versus accurately diagnosed cases. The percentage of calcifications retrieved was significantly different (p = 0.017). No underestimations were found among cases in which the entire mammographic lesion was removed at vacuum suction biopsy.
CONCLUSION. The cancer underestimation rate with vacuum suction biopsy was 9.5%. The underestimation rate for calcifications (16.3%) was significantly higher than that for masses (1.6%) (p = 0.007). The percentage of the lesion removed was an important factor in reducing underestimation, as reflected by the percentage of calcifications retrieved and the instances of complete resolution of the lesion seen on mammography.
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Underestimation at stereotactic core needle biopsy often results in the need for additional surgery. Patients with atypical ductal hyperplasia at stereotactic core needle biopsy will be advised to undergo a surgical biopsy. Patients with ductal carcinoma in situ at stereotactic core needle biopsy in whom invasive disease is subsequently found will often have to undergo additional breast or axillary node surgery. Therefore, minimizing underestimation would be desirable.
The vacuum suction device is an alternative to the automatic gun technique for performing stereotactic core needle biopsy. The vacuum suction method, using either 14- or 11-gauge probes, can obtain core samples that are substantially larger than those obtained with the 14-gauge needle and automatic gun [1, 4, 17]. Underestimation of cancer with vacuum suction biopsy has been shown to be less than that with the 14-gauge needle and automatic gun; however, underestimation still occurs [5, 9]. The purpose of this study was to determine the mammographic and histologic features of cancerous lesions underestimated with 11-gauge vacuum suction biopsy.
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Retrospective review to identify cases of atypical ductal hyperplasia, ductal carcinoma in situ, or invasive disease found at vacuum suction biopsy yielded 178 cases. The results of the stereotactic core needle biopsy were correlated with the subsequent surgical histology to identify cases in which cancer was underestimated by stereotactic core needle biopsy. Underestimated cancer cases were those in which either carcinoma was not diagnosed at stereotactic core needle biopsy (i.e., only atypical ductal hyperplasia was found) or invasive disease was not diagnosed at stereotactic core needle biopsy (i.e., only ductal carcinoma in situ was found). Accurately diagnosed cancer cases were defined as those in which the histologic diagnosis from the excisional biopsy was the same as or a lower stage than the diagnosis of the stereotactic core needle biopsy, including cases in which no residual carcinoma was found at surgery.
Cases reported as ductal carcinoma in situ with microinvasion at vacuum suction biopsy were considered invasive. Ductal carcinoma in situ cases reported as "possible invasion" were considered ductal carcinoma in situ, whereas those reported as having "probable invasion" were considered invasive. Pathologically, ductal carcinoma in situ with possible invasion was diagnosed when there were areas of ductal carcinoma in situ in which lobular involvement with stromal fibrosis and distortion suggested that invasion might be present. Ductal carcinoma in situ with probable invasion was diagnosed when there were areas of ductal carcinoma in situ in which periductal fibrosis and distortion of larger ducts suggested that microinvasion might be present. "Markedly atypical ductal hyperplasia" was used for borderline cases with a strong suggestion that intraductal carcinoma was present. This category included cases that qualitatively had the features of ductal carcinoma in situ but that were limited to one or two ductal profiles.
All core and surgical specimens were interpreted by a single pathologist experienced in breast pathology. Three levels were cut in each core specimen. Whenever discordance between the core and surgical histology occurred, review of both specimens was performed. In no case did the original pathologic interpretation change. Calcifications were identified pathologically.
Three separate analyses were performed to compare the accurately diagnosed and underestimated cases: the entire cancer group, the group of ductal carcinoma in situ alone, and the group of atypical ductal hyperplasia alone. The underestimated and the accurately diagnosed cases were compared in terms of mammographic features (mass, calcifications, or architectural distortion), size (as measured on the longest mammographic diameter), and number of core samples obtained during stereotactic core needle biopsy.
A retrospective review of the specimen radiographs and the mammograms obtained before biopsy was performed by an experienced breast radiologist to estimate the proportion of calcifications per lesion retrieved during vacuum suction biopsy. The calcification retrieval was considered low if less than 25%, moderate if 25-75%, and high if greater than 75% of the calcifications constituting the lesion were removed.
The mammographic findings at the time of needle localization for surgical excision were assessed retrospectively by an experienced breast radiologist. Cases in which the mammographic lesion was no longer visible at the time of needle localization were reviewed to compare the histologic findings at stereotactic core needle biopsy and surgery.
Two-by-two tables were analyzed using the chi-square test with Yates correction. Measured parameters between groups were compared using the Student's t test. Statistical significance was indicated by a p value equal to or less than 0.05. Statistical values were calculated using the SYSTAT, version 5.2, statistical package (Systat, Evanston, IL).
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Comparisons of the underestimated and accurately diagnosed cases for the entire cancer group, the ductal carcinoma in situ group, and the atypical ductal hyperplasia group are seen in Table 1. The underestimation rate for calcifications was 16.3% (14/86) and for masses was 1.6% (1/64). This difference is statistically significant (p=0.007).
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The mean sizes of the underestimated cases were not significantly different from those of the accurately diagnosed cases for the entire cancer group, the ductal carcinoma in situ group, and the atypical ductal hyperplasia group. Also, we found no significant difference in the number of core samples obtained in the underestimated cases compared with the accurately diagnosed cases in any group.
Of the 49 cases of ductal carcinoma in situ, invasive carcinoma was found in nine. Thus, the rate of underestimation for ductal carcinoma in situ was 18% (9/49). Of the underestimated ductal carcinoma in situ cases, almost half (4/9) were reported with "possible invasion" at vacuum suction biopsy. In comparison, only three of the 40 accurately diagnosed ductal carcinoma in situ cases were reported with possible invasion. The difference is statistically significant (p = 0.02). However, the positive predictive value of a diagnosis of "possible invasion" is only 57% (4/7).
Of the 26 cases of atypical ductal hyperplasia, six were found to harbor carcinoma, for a cancer underestimation rate of 23%. Of the six underestimated atypical ductal hyperplasia cases, five (83%) were reported as "markedly atypical" at vacuum suction biopsy. This is in contrast to the accurately diagnosed cases, for which only one (5%) of 20 was reported to be markedly atypical. This difference is statistically significant (p = 0.0006). The positive predictive value of a histologic diagnosis of "markedly atypical ductal hyperplasia" is thus 83% (5/6).
Specimen radiography was prospectively recorded (at the time of biopsy) as positive for retrieval of calcifications in all cases with calcifications in the study group (atypical ductal hyperplasia and cancer cases). Specimen radiographs and mammograms were available for review in all 14 underestimated calcification cases and 80 (93%) of the 86 accurately diagnosed (72 cancer and 14 atypical ductal hyperplasia) calcification cases. Quantification of the calcification retrieval revealed significantly greater (p = 0.017) retrieval in the accurately diagnosed group than in the underestimated group (Table 2).
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At the time of needle localization for surgery, the mammographic lesion was no longer seen in 12 cases (10 calcifications and 2 masses). The mean lesion size in these cases was 5.5 mm (range, 2-10 mm). Of these, seven (58%) had no residual disease at surgery (4 atypical ductal hyperplasia, 2 ductal carcinoma in situ, and 1 invasive carcinoma), three (25%) were concordant with the vacuum suction biopsy diagnosis (2 atypical ductal hyperplasia and 1 ductal carcinoma in situ), and two (17%) had less aggressive disease (only ductal carcinoma in situ found after invasive carcinoma was diagnosed at vacuum suction biopsy). Thus, all cases with no residual mammographic abnormality were accurately diagnosed at vacuum suction biopsy.
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Our data show that almost all (93%) underestimated cases were those presenting mammographically as calcifications. Of atypical ductal hyperplasia lesions that proved to be carcinoma at excision, Liberman et al. [18] also found a significantly higher percentage of calcifications than masses.
The underestimation rate has not been found to be related to the number of cores obtained. In our data, the number of cores was not statistically different in the underestimated and accurately diagnosed groups for the whole cancer group, the ductal carcinoma in situ group, or the atypical ductal hyperplasia group. This finding may be a result of small sample size, because we had only 15 underestimated cases. However, similar results were described by Brem et al. [2] for atypical ductal hyperplasia cases and Won et al. [14] for ductal carcinoma in situ cases. This might be explained by the fact that the number of cores obtained may not reflect the degree of thoroughness of sampling. That is, for some calcification cases, more cores may be required to successfully retrieve calcifications. The greater number of cores in these cases may not mean more adequate sampling, but initial failure to retrieve calcifications.
We found for calcification cases, the greater the proportion of the lesion removed, the less likely the chance of underestimation. Liberman et al. [15] similarly found no underestimations in five cases in which all calcifications were removed. The optimal number of cores to obtain with the 11-gauge vacuum suction device for calcification cases has not been determined. From our data, it appears that the more of the lesion that is removed, the better the concordance of vacuum suction biopsy with surgical histology.
Although no significant difference in the sizes of the underestimated and accurately diagnosed cases was found, there was a trend for increased size among the underestimated cases, especially the ductal carcinoma in situ underestimates. The smaller the lesion, the more chance there is for complete removal with the 11-gauge vacuum suction device and the less likely the chance of underestimation. Of the 12 lesions in which no residual mammographic abnormality was present at the time of surgery, no lesion was found to be underestimated. This finding is consistent with the results of Liberman et al. [19], who similarly found no underestimations among 15 carcinomas in which the mammographic lesion was noted to be gone immediately after vacuum suction biopsy.
One proposed criterion for differentiating ductal carcinoma in situ from atypical ductal hyperplasia is the involvement of atypical cells in two or more ducts, or size equal to or greater than 2 mm [20]. The differentiation of these two entities may, therefore, be an issue of quantity. Because all our cases were interpreted by a single breast pathologist, we cannot assess interobserver variability. Although there are proposed classification schemes for atypical ductal hyperplasia [21], variability in pathologists' interpretations of these borderline cases likely occurs [22]. In our underestimated atypical ductal hyperplasia cases, most (5/6) were diagnosed as markedly atypical at vacuum suction biopsy. Thus, it appears possible that subclassification of atypical ductal hyperplasia may allow some lesions to avoid surgical excision. Further studies may delineate which atypical ductal hyperplasia cases may not need to undergo surgical excision.
Although underestimation still occurs with the vacuum suction device and may be impossible to avoid completely, the data presented in this study help to clarify which cases are more likely to result in underestimation. Underestimation is significantly more likely to occur in cases of calcification than in cases of masses. The greater the proportion of the lesion removed, the less the underestimation. The percentage of calcifications retrieved was significantly different in the underestimated and in the accurately diagnosed cases. Likewise, lesions that were found mammographically to be completely resolved, were not found to be underestimations at the time of surgery. Underestimation of cancer may be suspected in many of the ductal carcinoma in situ cases (those reported as "possible invasion") and most atypical ductal hyperplasia cases (those reported as "markedly atypical"). This information should aid in patient management for physicians who perform these procedures.
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