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Breast Imaging |
1 From the Department of Diagnostic Radiology, Yale University School of Medicine, 333 Cedar St, New Haven, CT 06520. From the 1997 RSNA scientific assembly. Received August 11, 1998; revision requested September 25; revision received November 10; accepted January 11, 1999. Address reprint requests to C.H.L.
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: From July 1992 through December 1995, 355 of 540 cases (66%) in which SCNB yielded benign results were managed with follow-up mammography. Mammographic follow-up was available for 298 of these cases (84%). Follow-up mammography reports were reviewed. When a change was reported, pre- and postbiopsy mammograms, pathology reports, and results of subsequent mammographic follow-up were reviewed.
RESULTS: Mammographic change occurred in 21 of 298 cases (7%) at intervals of 6–55 months (mean, 20 months). Change occurred after initial mammographic stability in 10 of 21 cases. Repeat biopsy was performed in 18 of 21 cases. Malignancy was diagnosed in two cases: one mass that changed at 6 months and one case of microcalcifications that changed at 24 months. This represented a delayed false-negative rate of 2% (two of 105 malignancies among 540 biopsies).
CONCLUSION: A small percentage of cases diagnosed as benign with SCNB will change on follow-up mammograms, which may necessitate repeat biopsy. These results suggest that 6-month follow-up for cases that yield nonspecific benign results at SCNB and yearly screening mammography for cases with specific benign results is a reasonable management strategy.
Index terms: Breast, biopsy, 00.1267 • Breast neoplasms, diagnosis, 00.1267 • Breast radiography, utilization
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In addition, unlike in excisional biopsy, the aim of SCNB is to sample rather than completely remove the mammographic abnormality. Therefore, the potential exists for the lesion to change during follow-up, which at times prompts repeat biopsy. Follow-up mammograms are necessary to determine the stability of the remaining lesion in those cases in which SCNB yields benign histologic findings. The optimal mammographic follow-up strategy for these cases is yet to be determined, to our knowledge. The best strategy would balance the need for detecting false-negative cases as soon as possible against the inconvenience and added cost of short-interval follow-up examinations. The reported follow-up protocol for cases with benign results of SCNB varies, with some recommending short-interval follow-up for all such cases (6) and others recommending 12-month follow-up for all cases (9) or 6-month follow-up for some cases with benign results and 12-month follow-up for others (10).
The purpose of this study was to determine how often lesions diagnosed as benign with SCNB change at follow-up mammography, which type of lesion is likely to change, and when the change occurs in these lesions. This information should help determine the optimum management strategy for cases with benign results of SCNB and help determine the delayed false-negative rate among these cases.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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During the study, 540 SCNB procedures were performed at our facility in 472 patients. The patients were aged 31–84 years, with a mean age of 54 years. In 367 of the 540 biopsies (68%), benign histologic results were obtained for which the management recommendation was either short-interval or routine yearly mammographic follow-up. In 12 of these cases, the patient underwent further surgery despite the recommendation for mammographic follow-up. In five cases, this was done because of the patient's and/or the referring physician's unwillingness to accept the results of the SCNB. In another four cases, the lesion was excised along with a second lesion in proximity in the same breast, which was excised because of a diagnosis of atypical hyperplasia or because an insufficient sample was obtained at SCNB. In three cases, the lesion was removed when a malignancy elsewhere in the same breast was excised. Of the remaining 355 biopsies, 298 (84%) have mammographic follow-up information available.
Follow-up information was obtained through May 1998 from computerized mammography records at our facility, from outside facilities, from the referring physician, or from the patient herself. Follow-up examination was performed at our institution in 231 of the 298 cases (78%). In the remaining 67 cases (22%), follow-up mammograms were obtained at a number of outside facilities.
A substantial change in the mammographic appearance was defined as an increase in size for masses or an increase in number for calcifications and/or a more suspicious morphology for both masses and calcifications. In cases in which a substantial change was reported, the original and follow-up mammograms were obtained and independently reviewed by one of the authors (C.H.L.) for the initial mammographic finding, the type and magnitude of change, and the interval between the SCNB and the mammographic change. Lesion size was recorded as the greatest diameter among the three dimensions. The histologic results of tissue obtained at the time of initial SCNB and subsequent biopsy were noted.
At our facility, short-interval follow-up mammography is usually recommended despite lesions in which a nonspecific benign result concordant with the mammographic impression is obtained. Our short-interval follow-up protocol consists of a unilateral mammographic examination at 6 months, then bilateral diagnostic mammographic examinations at 12 and 24 months. If stability is documented at these examinations, the patient is advised to resume routine yearly screening at 36 months. When the lesion that is being followed up consists of calcifications, magnification views are usually obtained. When SCNB yields a specific benign result that is concordant with the mammographic finding, the management recommendation is usually screening mammography at 1 year. Immediate biopsy is recommended for benign results when atypical hyperplasia, lobular carcinoma in situ, radial scar, or insufficient material is obtained or when there is a perceived discrepancy between the mammographic impression and the histologic result or when the pathologist recommends that more tissue be obtained for a definitive diagnosis.
Histologic results considered to be nonspecific benign findings include fibrocystic changes, apocrine metaplasia, benign breast tissue, and fibrous breast tissue. Specific benign diagnoses include fibroadenoma, lymph node, and cyst. The categories of specific and nonspecific benign findings serve as general guidelines for management decisions, and the final recommendations are made after consideration of the histologic, mammographic, and clinical features of each case. Therefore, occasionally, when a nonspecific benign result is obtained but the level of suspicion based on the mammographic finding is low, a 12-month follow-up examination might be recommended.
Patients in whom no mammographic follow-up or less than 12 months of mammographic follow-up was obtainable were cross-referenced with the Connecticut Tumor Registry (Connecticut Department of Public Health, Hartford) to attempt to identify possible cases of breast cancer that may have been diagnosed subsequent to the SCNB. The total number of malignancies diagnosed in all patients who underwent SCNB during the study was determined to calculate the false-negative rate. The Student t test was used to compare differences in the timing of change of masses and of calcifications.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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For the 298 cases, the duration of mammographic follow-up was 5–65 months, with a mean of 33 months. Mammographic follow-up of 22 months or longer or histologic results of repeat biopsy were available for 253 cases (85%). Of the 45 cases with less than 22 months of follow-up, 25 were masses, 19 were calcifications, and one was a mass with calcifications. Seven of these had follow-up of 5–11 months, 20 had follow-up of 12–17 months, and the remaining 18 had follow-up of 18–21 months. Among the 180 cases in which short-interval mammography was recommended, mammography was performed in 110 (61%) within 9 months of the SCNB procedure. Among the 118 cases in which follow-up mammography at 12 months was recommended, mammography was performed in 69 (58%) within 15 months of the biopsy. In 169 (57%) of the 298 cases, at the time this article was written, either 3 years of mammographic follow-up had been completed or the recommended follow-up was being complied with.
Twenty-one (7%) of the 298 cases showed a substantial change on follow-up mammograms. These included 12 cases of calcifications, which represented 11% of all of the cases of calcifications for which follow-up information was available, and nine masses, which represented 5% of the masses in this series. Details of these 21 cases are presented in Tables 1 and 2. The ages of the women in whom the lesions changed ranged from 31 to 74 years, with a mean age of 48 years. The mammographic change in all of the cases of calcifications was an increase in the number of calcifications. None of the cases with an increased number of calcifications showed a more suspicious morphology. All of the masses that changed increased in size, with the amount of increase ranging from 1 to 10 mm and a mean change of 4.7 mm. One mass became palpable and increased in size at 18 months. One mass increased only minimally in size but became more spiculated.
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In 18 of the 21 cases that changed, repeat biopsy was performed. The correlation between SCNB histologic results and the repeat biopsy results in these cases is detailed in Table 3. Representative cases are shown in Figures 1 and 2. In two cases, repeat SCNB was performed and again yielded benign results. In both these cases, continued mammographic stability has been documented for 9 and 15 months at the time this article was written.
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The interval between the SCNB and mammographic change for the 21 cases was 6–55 months, with a mean of 20 months. The time of the first mammographic follow-up examination for the 21 cases ranged from 5 to 29 months, with a mean of 13 months. Ten of the 21 cases showed either a decrease in the size of the mass or in the number of calcifications or no change on the first follow-up mammogram but an increase on a subsequent mammogram. The time in which masses changed was 6–24 months, with a mean of 16 months. The time in which calcifications changed was 12–55 months, with a mean of 23 months. This difference was not statistically significant (P = .129). None of the cases manifesting as calcifications changed before 12 months, including the one false-negative case. Of the nine masses, two changed at 6 months, including the false-negative case. The second mass that changed at 6 months was a cellular fibroadenoma, which was diagnosed with SCNB. In this case, a 6-month follow-up examination was recommended despite the specific benign result because of the cellularity of the lesion. None of the masses changed after 24 months.
Cross-reference with the Connecticut Tumor Registry did not reveal any cases of breast carcinoma diagnosed among the 64 women in our series for whom no mammographic follow-up or less than 12 months of follow-up information was available. Of the 540 SCNB procedures performed during the study, 105 (19%) revealed malignancy. Ninety-two of these cancers were diagnosed initially with SCNB. Thirteen were diagnosed with excisional biopsy immediately following the SCNB procedure because of insufficient sampling (three cases) or a high-risk lesion such as atypical hyperplasia (10 cases). The other two cases were those described in this report in which the diagnosis was made after a mammographic change at 6 and 24 months. If only these two cases are considered to be delayed false-negative cases, the delayed false-negative rate for our series was 2% (two of 105).
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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A large percentage of the lesions that changed in our series (48%) were determined with histologic SCNB findings to be fibroadenomas. When a previously diagnosed fibroadenoma increases in size, the possibility that it actually represents a phyllodes tumor or that a malignancy is present within or adjacent to the fibroadenoma must be considered (11,12). However, these entities are relatively rare, whereas growth of fibroadenomas has been well described (13–15). Meyer et al (14) reported mammographically documented growth in 22 of 254 fibroadenomas (9%) that were subsequently excised, and, in another series (15), four of 279 (1%) clinically palpable fibroadenomas increased in size and were subsequently excised.
Malignancy has not been diagnosed among our cases of fibroadenomas that changed, although one was found at excision to be associated with atypia within the fibroadenoma. Our series was too small to definitively conclude that repeat biopsy is unnecessary for lesions diagnosed as fibroadenomas with SCNB that have changed by follow-up mammography. However, findings in these cases suggest that continued short-interval mammographic follow-up may be a reasonable alternative to repeat biopsy in premenopausal women. Another alternative to excisional biopsy or continued mammographic surveillance for these women might be repeat SCNB with an 11-gauge vacuum-assisted device. Further studies are needed to determine if this is a valid management strategy.
Change on a follow-up mammogram occurred at 6 months in two cases manifesting mammographically as masses, including one of the false-negative cases. None of the cases of calcifications that were followed up showed an increase before 12 months, including the one false-negative case that was seen mammographically as calcifications. Three cases of calcifications changed after 24 months of follow-up, whereas none of the masses did. The difference in the mean time of change for masses and calcifications was not statistically significant.
Our results suggest that recommending 6-month follow-up mammography is a prudent course of action for noncalcified masses when nonspecific benign results are obtained with SCNB. Because the difference in the time of change for masses and calcifications was not significantly different, the recommendation in cases of calcifications that yield nonspecific benign results should probably also be 6-month follow-up mammography, despite the fact that none of the calcification cases in our series changed prior to 12 months.
Since none of the masses in our series changed after 24 months, our results suggest that women with masses who undergo short-interval follow-up can undergo yearly screening after 24 months of stability has been documented. The interval before routine yearly screening mammography can be recommended may need to be longer for calcifications, which usually require magnification views to be adequately followed up.
Our results show that stability or an actual decrease in size or number on the initial follow-up mammogram does not necessarily exclude change at a subsequent examination, nor does it exclude the presence of malignancy. In 11 (52%) of the 21 cases that changed in our series, the first postbiopsy mammogram showed stability, but change was found on a subsequent follow-up mammogram. This occurred in one of the false-negative cases that manifested as calcifications. The calcifications were actually decreased in number on the first follow-up mammogram obtained at 12 months but were increased in number at 24 months. This emphasizes the importance of continued follow-up of lesions diagnosed as benign with SCNB, particularly those that manifest mammographically as calcifications.
While the false-negative rate of SCNB as determined by means of correlation with immediate surgical excision has been evaluated by several investigators, reports of false-negative cases detected after mammographic follow-up rather than immediate surgery (the delayed false-negative rate) have, until recently, been limited (6–8,16,17). In a study (7) of 84 cases with benign SCNB results followed up clinically and mammographically for a mean of 24 months, no delayed false-negative cases were found.
In a multiinstitutional study, Parker et al (6) reported on 2,429 cases with at least 6 months of mammographic follow-up. Of these, 2,402 cases showed no change, 27 showed change at follow-up, and five malignancies were diagnosed. In addition, Parker et al (16) also reported an additional four cancers detected among their cases after an additional year of follow-up. The total length of follow-up was not specified in this report.
Fajardo (17) reported on three cases of malignancy diagnosed among a total of 400 cases, 271 of which were followed up mammographically for 2 years after a benign SCNB diagnosis. These false-negative cases were discovered at 6, 8, and 13 months after SCNB. It is difficult to precisely determine the false-negative rate in this report, as the total number of cancers diagnosed in the group was not explicitly given. In the series of Jackman et al (8), two of the 26 lesions that showed mammographic progression at follow-up were malignant at repeat biopsy. One was a mass that showed progression at 18 months and proved to be a stage I invasive ductal carcinoma, and the second was a cluster of calcifications that increased at 6 months and was diagnosed as ductal carcinoma in situ at repeat biopsy. Their delayed false-negative rate was 1.2% (two of 161 carcinomas).
We had a delayed false-negative rate of 2%. It is possible that additional malignancies have occurred among cases in our series for which no follow-up information is available. This is thought to be unlikely, however, given that no such cases have been identified by means of cross-reference with the Connecticut Tumor Registry. Malignancy may yet be diagnosed in those five cases in which repeat SCNB or continued mammographic follow-up examination rather than excisional biopsy was performed after mammographic change. However, this is thought to be unlikely given that continued mammographic stability has been documented in these cases. It is also possible that additional malignancies will eventually be identified among the 44 cases in our series with less than 22 months of follow-up.
Comparing the delayed false-negative rate for SCNB with that for excisional biopsy of nonpalpable breast lesions is problematic in that, in most series of needle-localized lesions in which excision is performed, unsuccessful excision rates are reported rather than actual false-negative rates based on long-term follow-up of cases in which unsuccessful excisional biopsy has been performed.
Jackman and Marzoni (18) recently reviewed this literature extensively. Misses at the time of excisional biopsy are often apparent on the radiograph of the specimen, and many patients in whom misses occur will undergo immediate repeat excision (19). However, radiographs of specimens are not always obtained and do not always reliably indicate if a lesion, particularly a noncalcified mass, has indeed been excised (20). It is likely that the delayed false-negative rate for needle-localized excisional biopsy, although very low, is not zero.
In the cases in our series, biopsy was performed with the 14-gauge automated biopsy device and a mean of only six passes per case. With the vacuum-assisted biopsy device, more tissue is usually removed (21), and it is possible that the optimal mammographic follow-up protocol for cases in which SCNB is performed with this technique will be different from that for cases in which biopsy is performed with the automated biopsy gun. Long-term follow-up studies are needed to determine this and to determine if the use of the vacuum-assisted device will decrease the delayed false-negative rate (22).
In conclusion, we found that 7% of cases that yielded benign results of SCNB had changed by follow-up mammography which prompted repeat biopsy in 6%. This was particularly likely in young women in whom a fibroadenoma was diagnosed with SCNB findings. The change did not necessarily occur on the first posttreatment mammogram and tended to occur later with calcifications rather than with masses, although the difference was not statistically significant. We found a 2% delayed false-negative rate after a mean of 33 months of mammographic follow-up. On the basis of our results, we believe that 6-month follow-up mammography for cases with nonspecific benign diagnoses and routine yearly screening mammography for cases with specific benign histologic results is a reasonable management strategy. Because the mammographic change sometimes occurred after the first follow-up examination, patients and referring physicians need to be aware of the importance of continued mammographic follow-up after a benign diagnosis is obtained with SCNB.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, C.H.L.; study concepts, C.H.L., I.T.; study design, C.H.L.; definition of intellectual content, C.H.L.; literature research, C.H.L.; clinical studies, C.H.L., L.E.P., L.J.H., I.T.; experimental studies, C.H.L., L.E.P., L.J.H., I.T.; data analysis, C.H.L.; statistical analysis, C.H.L.; manuscript preparation, C.H.L.; manuscript editing, C.H.L., L.E.P., L.J.H., I.T.; manuscript review, L.E.P., L.J.H., I.T.
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References |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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