Evaluation of Breast Imaging Reporting and DataSystem Category 3 Mammograms and the Use ofStereotactic Vacuum-Assisted Breast Biopsy in aNonacademic Community Practice

Angela Mendez, M.D.

Fernando Cabanillas, M.D.

Miguel Echenique, M.D.

Keyvan Malekshamran, M.D.

Iris Perez, R.T.

Edwin Ramos, M.D.

Auxilio Mutuo Cancer Center, Hospital Auxilio Mu-tuo, San Juan, Puerto Rico.

Address for reprints: Fernando Cabanillas, M.D.,Auxilio Mutuo Cancer Center, Hospital Auxilio Mu-tuo, Ave. Ponce de Leon 725, San Juan, PuertoRico 00918; Fax: (787) 771-7941; E-mail:cabanillas@auxilio.com

Received September 15, 2003; revision receivedNovember 10, 2003; accepted November 13,2003.

BACKGROUND. Breast Imaging Reporting and Data System (BI-RADS) Category 3

represents ‘probably benign’ mammographic abnormalities requiring close follow-

up, but biopsies sometimes are performed on Category 3 abnormalities. Contro-

versy exists as to when these biopsies are justified. The goals of the current study

were to evaluate the use of stereotactic vacuum-assisted breast biopsy (SVABB) for

BI-RADS 3 lesions in a nonacademic community hospital– based practice, to eval-

uate the false- negative rate of Category 3 mammograms, and to determine

whether any specific lesions misinterpreted as BI-RADS 3 abnormalities might

commonly be associated with malignant disease.

METHODS. From August 2000 to December 2002, the authors performed 947 SVABB

procedures on 911 patients. They focused on 156 SVABBs of BI-RADS 3 abnormal-

ities.

RESULTS. Of 634 SVABB procedures requested by outside sources, 114 (18%) were

performed for BI-RADS 3 abnormalities, compared with 42 (13%) of 313 SVABB

procedures that were performed based on mammographic findings at the authors’

practice (P � 0.075). After SVABB, 7 of 156 patients with BI-RADS 3 lesions were

diagnosed with breast carcinoma and 1 was diagnosed with atypical ductal hyper-

plasia. Therefore, the false-negative rate of BI-RADS 3 mammograms was 4.5% (i.e.,

7 of 156 patients). Patients with linear microcalcifications had the highest rate of

cancer (4 of 14 [29%]) compared with patients without microcalcifications (1 of 64

[1.5%]) and patients with nonlinear microcalcifications (2 of 69 [2.9%]).

CONCLUSIONS. The use of SVABB for BI-RADS 3 lesions reflected uncertainty

regarding the potential for a diagnosis of malignant disease rather than the finan-

cial incentive of performing a biopsy. SVABB was not necessary for patients with

BI-RADS 3 lesions without microcalcifications or for patients with nonlinear mi-

crocalcifications. Lesions with linear (casting or branching) microcalcifications

should not be considered BI-RADS 3 abnormalities. Cancer 2004;100:710 – 4.

© 2004 American Cancer Society.

KEYWORDS: mammogram, Breast Imaging Reporting and Data System Category 3,stereotactic breast biopsy, percutaneous breast biopsy, breast carcinoma biopsy.

The Breast Imaging Reporting and Data System (BI-RADS) wasproposed by the American College of Radiology1 to decrease the

ambiguity regarding descriptions of mammographic lesions and toprovide a common language to unambiguously describe the level ofsuspicion and recommended follow-up for a mammographic lesion.Annual follow-up is recommended for patients with lesions classifiedas BI-RADS Category 1 (negative mammogram) or 2 (benign findings).

710

© 2004 American Cancer SocietyDOI 10.1002/cncr.20017

A 6-month follow-up has been recommended for pa-tients with lesions assigned a BI-RADS Category 3(probably benign) whereas a biopsy is suggested forpatients with lesions classified as Category 4 (suspi-cious) or 5 (highly suggestive of malignancy). In spiteof these guidelines, for various reasons, biopsies areperformed for some BI-RADS 3 lesions, and this topichas been a matter of considerable debate and contro-versy.2,3 Many do not realize that a lesion should notbe categorized as a BI-RADS 3 abnormality before animaging workup, which would include magnificationviews for patients with microcalcifications, is per-formed. After a thorough imaging workup revealingBI-RADS 3 findings, some legitimate reasons for per-forming a biopsy are the presence of malignant tu-mors in the same breast or the opposite breast, de-mands from extremely apprehensive patients andfrom patients planning a future pregnancy or aug-mentation or reduction surgery, and uncertainty as towhether the patient will comply with the requiredregular mammographic follow-up examinations; anegative stereotactic vacuum-assisted breast biopsy(SVABB) will result in less-frequent follow-up. A lesslegitimate reason is the fear of a malpractice suit if adiagnosis of malignancy is missed. In addition, someinvestigators believe that a number of biopsies forBI-RADS 3 lesions might be driven by profit motives;to our knowledge, this hypothesis has not been objec-tively evaluated in the existing literature.

The SVABB technique is being used more fre-quently because, compared with excisional biopsy, itrepresents a minimally invasive, faster, and less ex-pensive method for sampling nonpalpable abnormal-ities observed on mammography but not on sonogra-phy. If a lesion is observed on sonography, ourapproach is to perform a biopsy using sonographicguidance, because this option is less expensive. If thelesion is not observed on a breast sonogram, the bi-opsy is performed with either stereotactic guidance orby wire localization. For lesions not observed on asonogram, we prefer the stereotactic method, becauseit is faster, less expensive, less painful, less invasive,and can be performed easily in the outpatient setting.SVABB is indicated most commonly for BI-RADS 4lesions. Patients with BI-RADS 5 lesions frequently arereferred directly for excisional biopsy, because of theexpected high frequency of malignancy. However, inmany instances, patients with BI-RADS 5 lesions un-dergo percutaneous biopsies to allow appropriate sur-gical planning and one surgical procedure.

We initiated the current study with three goals inmind: 1) to evaluate the use or misuse of SVABB forBI-RADS 3 lesions in a nonacademic hospital– basedpractice (Auxilio Mutuo Cancer Center, Hospital Aux-

ilio Mutuo, San Juan, Puerto Rico); 2) to evaluate thefalse-negative rate of Category 3 mammograms; and 3)to determine whether there are any specific lesionsmisinterpreted as BI-RADS 3 abnormalities that mightcommonly be associated with malignant disease.

MATERIALS AND METHODSFrom August 2000 to December 2002, we performed947 SVABB procedures on 911 patients using an up-right Mammomat 1000/3000 Nova Opdima digital bi-opsy and spot imaging system unit (Siemens-ElemaAB, Solma, Sweden). The 11-gauge needle used forthese biopsies was a Mammotome probe MST 11(Ethicon Endo Surgery; Cincinnati, OH). Specimen ra-diography was performed routinely on all samples,and mammographic lesions were classified into fourcategories: 1) microcalcifications; 2) asymmetric den-sity; 3) circumscribed mass; and 4) spiculated mass.The major indication for SVABB in the current serieswas a BI-RADS 4 mammogram (n �757, or 80% of allprocedures). However, 156 SVABB procedures wereperformed for patients with BI-RADS 3 lesions.

Hospital Auxilio Mutuo is a nonprofit, private in-stitution with tertiary facilities and 510 approved beds.It is located in a metropolitan area and draws patientsfrom the whole island. Approximately 6% of all newcancer cases on the island and 22% of those in themetropolitan area are diagnosed at our center. TheWomen’s Imaging Center, located within our institu-tion, houses facilities for three mammography rooms,one room for stereotactic biopsies, and three roomsfor breast sonograms. It provides services to our ownpopulation of patients as well as for those referredfrom outside sources.

Before SVABB was performed, all patients wereexamined by one of three radiologists assigned to theWomen’s Imaging Center, and all films were reviewed.The three radiologists are experienced in the field ofmammography and devote 80% of their time to breastimaging. A BI-RADS category was assigned beforeSVABB was performed. Either a surgeon or a radiolo-gist performed the SVABB procedure. During the cur-rent study period, four surgeons and three radiologistsperformed SVABB procedures. All surgeons and radi-ologists held credentials granted by the faculty by-laws committee; the criteria for granting credentials tosurgeons are virtually identical to those proposed bythe American College of Radiologists.4 Whenever thesurgeon performed SVABB, the radiologist assistedwith targeting. Specimens were X-rayed before beingsubmitted for pathologic evaluation. Subsequently, allpathology reports were reviewed by the radiologist,who assessed concordance/discordance.

A BI-RADS category was assigned using the inter-

BI-RADS 3 and Stereotactic Breast Biopsy/Mendez et al. 711

pretation provided by the first radiologist who readthe films, either the radiologist from another institu-tion or the radiologist from our institution. Of the 947mammograms administered before SVABB, 313 wereperformed at our center and 634 were performed atother centers before the patient was referred to ourcenter for SVABB.

False-negative findings were defined as BI-RADS 3findings for which stereotactic biopsy yielded positiveresults for malignancy. A positive result on repeatbiopsy of a BI-RADS 3 abnormality also was consid-ered to indicate a false-negative mammogram. A false-negative result also was recorded for any initial biopsyof a BI-RADS 3 lesion that was considered to be aninadequate tissue sample and that required a repeatbiopsy that was positive for breast carcinoma. In ad-dition, BI-RADS 3 lesions that upon follow-up re-quired a repeat biopsy that was positive were consid-ered to represent false-negative findings. The tumorregistry also was evaluated in an attempt to find tu-mors that subsequently were diagnosed as breast car-cinoma.

Permission was obtained from the local institu-tional review board for publication of the findingssummarized in the current study.

RESULTSUse of SVABB in BI-RADS 3 and 4 LesionsWe performed 947 SVABB procedures, of which 634were requested by outside sources. Of these 634 SVABBprocedures, 114 (18%) were for BI-RADS 3 lesionscompared with 42 (13%) of the 313 that originatedfrom our practice (P � 0.075). The use of SVABB forBI-RADS 4 lesions was significantly more common inour practice than it was elsewhere (262 [84%] of 313 vs.495 [78%] of 634; P � 0.04).

We also compared the rate of cancer diagnosis forpatients with BI-RADS 3 lesions who were referred forSVABB from an outside source with the correspondingrate for patients in our practice. The results were al-most identical in both cases, with rates of approxi-mately 5% (Table 1).

False-Negative Rate in BI-RADS 3 LesionsA BI-RADS 3 mammogram with a stereotactic biopsypositive for carcinoma was defined as a false-negativemammogram. After the SVABB procedure, 7 of the 156patients with BI-RADS 3 lesions were diagnosed withbreast carcinoma and 1 was diagnosed with atypicalductal hyperplasia (Table 1). Therefore, the false-neg-ative rate, including only patients diagnosed with can-cer, is 4.5% (i.e., 7 of 156 patients).

Correlation of Type of Lesion with Diagnosis ofMalignancyWe classified patients with BI-RADS 3 abnormalitiesaccording to mammographic lesion type (i.e, micro-calcifications, asymmetric density, circumscribedmass, or spiculated mass). Of the 156 biopsies per-formed for BI-RADS 3 lesions, 92 (59%) were per-formed for microcalcifications, 25 (16%) for an asym-metric density, 37 (24%) for a circumscribed mass, and2 (1.3%) for a spiculated mass. One of the two patientswith a spiculated mass was known to have undergonea previous biopsy, and it was believed that the lesionprobably was due to scar tissue. For that reason, thelesion was classified as a BI-RADS 3 abnormality. Thesecond patient was believed to have a radial scar andshould have been assigned a BI-RADS 4 classificationrather than a BI-RADS 3 classification. The results ofSVABB confirmed the presence of scar tissue in thefirst patient, and the second patient was diagnosedwith proliferative fibrocystic disease.

Of the seven cases of malignant disease, six wereassociated with microcalcifications. Ninety-one pa-tients had microcalcifications. Of these 91 patients, 6(6.5%) had malignant disease, compared with 1 of 65patients without microcalcifications (1.5%) who hadmalignant disease (P � 0.13; Table 2). We then focusedon the pattern of microcalcifications to determinewhether a correlation with malignancy or atypia ex-isted. Information on microcalcification type wasavailable for 83 of the 92 patients. Patients with alinear pattern of distribution had the highest rate of

TABLE 1Histologic Findings in BI-RADS Category 3 Mammograms Accordingto Source of Referral

Source ofSVABBreferral No.

Breastmalignancy (%) Atypia (%) Total (%)

Our practice 42 2 (4.8) 0 2 (4.8)Outside source 114 5 (4.4) 1 (0.9) 6 (5.3)

BI-RADS: Breast Imaging Reporting and Data System; SVABB: stereotactic vacuum-assisted breast

biopsy.

TABLE 2Histologic Findings According to Absence/Presence ofMicrocalcificationsa

Lesion No. Malignant disease (%)

Any type of microcalfication 91 6 (6.5)No microcalcifications 65 1 (1.5)

a P � 0.13 for no microcalcifications versus microcalcifications.

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malignancy (29% [4 of 14]) compared with patientswith other types of microcalcifications (4% [3 of 69];Table 3). This observation was statistically significant(P � 0.009).

DISCUSSIONSixteen percent (156 of 947) of patients at our practicewith BI-RADS 3 lesions underwent SVABB. This is amuch higher rate compared with other series, inwhich only 3– 8% of patients with BI-RADS 3 lesionsunderwent SVABB (Table 4). To gain more insight intothe reason for the high rate of biopsy, we evaluated thesource of referral for the biopsy as a variable. Wedetermined that the proportion of patients referredfrom outside sources for SVABB was higher (18%) thanthe proportion of patients referred from our practice(13%). Because there is no financial incentive for theseoutside referrals, it is logical to conclude that in ourcommunity, profit was not the major reason for thehigh rate of biopsy for patients with BI-RADS 3 lesions.Other possible factors include the deteriorating localmalpractice climate in the island, cultural or socio-logic issues, and, perhaps, an incomplete awareness inthe medical community of the indications for biopsy.During the past decade, the number of malpracticesuits in Puerto Rico has increased substantially, andonly a maximum insurance coverage of $100,000 perincident is available. Sociologic issues that might im-

pact the performance of biopsies for BI-RADS 3 le-sions include a low level of education for a fraction ofpatients who might not return in 6 months for a fol-low-up mammogram. However, it is not possible toconclusively identify from the current study the mostlikely explanation for the disproportionately high rateof SVABB for BI-RADS 3 lesions.

BI-RADS 3 mammograms must be considered toessentially represent negative findings, because Cate-gory 3 lesions are defined as ‘probably benign abnor-malities’. For this reason, if the final outcome is adiagnosis of malignant disease, the mammogrammust represent false-negative findings. The literaturequotes a false-negative rate ranging from 0.5% to 2%for BI-RADS 3 lesions. However, these figures arebased on follow-up mammograms and not on system-atic biopsies.5,6 The false-negative rate for BI-RADS 3mammograms at our institution was 4.5% (7 of 156;Table 1). Figure 1 shows an example of false-negativemammographic results interpreted as BI-RADS 3 find-ings. Table 5 compares our results with those fromother series in which SVABB was performed for BI-RADS 3 lesions. To perform a fair comparison, onlyseries that used SVABB were considered, and we ex-cluded series in which data were derived from sono-graphically directed biopsies or other types of biop-sies. The study performed by Margolin et al.,8 whichinvolved sonographically guided biopsies as well asSVABB, was included; for that series, we extracted thedata on patients who underwent SVABB. When weadded the results of all 5 published series, there were6 of 213 (2.8%) false-negative results, compared with 7

TABLE 3Histologic Findings According to Microcalcification Typea

Lesion No. Malignant disease (%) Atypia (%)

Linear microcalcifications 14 4 (29) 0Nonlinear microcalcifications 69 2 (2.9) 1 (1.5)

a P � .007 for diagnosis of malignancy for nonlinear versus linear microcalcifications.

TABLE 4Proportion of Patients with BI-RADS Category 3 Lesions WhoUnderwent SVABB in the Current Series Compared with OtherPublished Series

Study Institution type

No. of patientsundergoingSVABB (%)

Current series Community hospital 156/947 (16)Berube et al., 19987 Academic center 16/495 (3)Margolin et al., 20018 Community hospital 16/321 (5)Tate et al., 20019 Community hospital 87/1088 (8)Travade et al., 200210 Community hospital 12/206 (6)

BI-RADS: Breast Imaging Reporting and Data System; SVABB: stereotactic vacuum-assisted breast

biopsy.

FIGURE 1. Left medial lateral (LML) magnification view. A cluster of micro-

calcifications can be seen in the left breast at the 12 o’clock position (arrows).

Stereotactic biopsy revealed ductal carcinoma in situ. The findings on this film

originally were classified at another institution as Breast Imaging Reporting and

Data System 3 abnormalities.

BI-RADS 3 and Stereotactic Breast Biopsy/Mendez et al. 713

of 156 (4.5%) in the current series (Table 1). Thisdifference is not statistically significant (P � 0.28).

Despite the lack of a significant difference in thefalse-negative rate between the current series and oth-ers, we set out to further investigate patients at ourinstitution who had positive biopsies to attempt toidentify a subset of patients with BI-RADS 3 lesionswho had a high rate of malignant disease. We foundthat of the seven patients with positive SVABB find-ings, six had microcalcifications. Stated differently,there were 92 patients with BI-RADS 3 lesions who hadmammographic microcalcifications. Six (6.5%) ofthese patients had positive SVABB findings, comparedwith only one (1.5%) patient without microcalcifica-tions (P � 0.13; Table 2). We then classified patientswith microcalcifications as patients with linear distri-butions or patients with other microcalcification types(Table 3). Data on microcalcification type were avail-able for 83 of 92 patients. Fourteen patients had lineardistributions, and 4 (29%) of these 14 were diagnosedwith malignant disease (Table 3). This result was instriking contrast with the finding that only 2 of 69patients (2.9%) with other types of microcalcificationshad positive findings on SVABB. This difference wasstatistically significant (P � 0.007; Table 3).

In conclusion, SVABB for BI-RADS 3 lesions isoverused in our community. This overuse may beattributable to uncertainty regarding the diagnosis ofmalignant disease or to other factors, such as fear of

malpractice litigation, rather than to the financial in-centive to perform a biopsy. Performing a biopsy forBI-RADS 3 lesions without microcalcifications or withnonlinear microcalcifications is not necessary unlessother justifications exist. If, from this point onward,we were to stop performing such biopsies, we wouldobserve a reduction of 8% in the number of SVABBprocedures currently being performed. Finally, in viewof the high frequency of positive findings in patientswith linear microcalcifications, radiologists at our in-stitution, as well as others, should not consider thesepatients to have BI-RADS 3 lesions, but rather BI-RADS 4 lesions.

REFERENCES1. American College of Radiology. Breast imaging reporting

and data system, 3rd edition. Reston, VA: American Collegeof Radiology, 1998.

2. Sickles EA, Parker SH. Appropriate role of core breast biopsyin the management of probably benign lesions. Radiology.1993;188:315.

3. Logan-Young WW, Janus JA, Destounis SV, Hoffman NY.Appropriate role of core breast biopsy in the management ofprobably benign lesions. Radiology. 1994;190:313–314.

4. American College of Surgeons and American College of Ra-diology. Physician qualifications for stereotactic breast bi-opsy: a revised statement. Bull Am Coll Surg. 1998;83:30 –33.

5. Varas X, Leborgne F, Leborgne J. Nonpalpable, probablybenign lesions: role of follow up mammography. Radiology.1992;184:409 – 414.

6. Sickles E. Periodic mammographic follow up of probablybenign lesions: results of 3184 consecutive cases. Radiology.1991;79:463– 468.

7. Berube M, Curpen B, Ugolini P, Lalonde L, Ouimet-Oliva D.Level of suspicion of a mammographic lesion: use of fea-tures defined by BI-RADS lexicon and correlation with large-core breast biopsy. Can Assoc Radiol J. 1998;49:223–228.

8. Margolin FR, Leung JW, Jacobs RP, Denny SR. Percutaneousimaging-guided core breast biopsy: 5 years’ experience in acommunity hospital. AJR Am J Roentgenol. 2001;177:559 –564.

9. Tate PS, Rogers EL, McGee EM, et al. Stereotactic breastbiopsy: a six-year surgical experience. J Ky Med Assoc. 2001;99:98 –103.

10. Travade A, Isnard A, Bagard C, et al. Stereotactic 11-gaugedirectional vacuum-assisted breast biopsy: experience with249 patients. J Radiol. 2002;83:1063–1071.

11. Obenauer S, Fischer U, Baum F, Dammert S, Fuzesi L,Grabbe E. [Stereotactic vacuum core biopsy of clusteredmicrocalcifications classified as B1-RADS 3]. Rofo FortschrGeb Rontgenstr Neuen Bildgeb Verfahr. 2001;173:696 –701.

TABLE 5False-Negative Rate for BI-RADS Category 3 Findings in the CurrentSeries Compared with Other Published Series Involving SVABB

Study No. of false-negative results (%)

Current series 7/156 (4.5)Berube et al., 19987 0/16 (0)Margolin et al., 20018 1/16 (6.3)a

Tate et al., 20019 2/87 (2.3)Travade et al., 200210 0/12 (0)Obenauer et al., 200111 3/82 (3.7)

BI-RADS: Breast Imaging Reporting and Data System; SVABB: stereotactic vacuum-assisted breast

biopsy.a For the purposes of comparison, we included only stereotactic biopsy findings and excluded sono-

graphically directed biopsy findings from this series.

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