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10.1245/s10434-006-9212-8
Annals of Surgical Oncology 14:704-711 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Predictive Value of Breast Lesions of "Uncertain Malignant Potential" and "Suspicious for Malignancy" Determined by Needle Core Biopsy

Mary F. Dillon, MB1, Enda W. McDermott, MCh1, Arnold D. Hill, MCh1, Ann O’Doherty, MB2, Niall O’Higgins, MCh1 and Cecily M. Quinn, MD3

1 Department of Surgery, St Vincent’s University Hospital, Elm Park, Dublin 4, Ireland
2 Department of Radiology, St Vincent’s University Hospital, Elm Park, Dublin 4, Ireland
3 Department of Pathology, St Vincent’s University Hospital, Elm Park, Dublin 4, Ireland

Correspondence: Address correspondence and reprint requests to: Mary F. Dillon, MB; E-mail: maryfdillon{at}hotmail.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: The optimum management of patients whose needle core biopsy (NCB) results are of "uncertain malignant potential" (B3) or "suspicious for malignancy" (B4) is unclear. This study correlates B3 and B4 NCB findings with excision histology to determine associated rates of malignancy.

Methods: All NCBs categorized as B3 or B4 were identified from a series of 3729 NCBs. Results of biopsies were reported as normal/nondiagnostic (B1), benign (B2), uncertain malignant potential (B3), suspicious but not diagnostic of malignancy (B4), or malignant (B5) according to the B classification system. B3 lesions included atypical intraductal epithelial proliferations (AIEPs), lobular neoplasia, papillary lesions, radial scars, and potential phyllodes tumors. Histological concordance between NCB and excision specimen was analyzed.

Results: A total of 211 B3 lesions and 51 B4 lesions were identified during the study period. The open biopsy rate after a B3/B4 finding was 86% (n = 226). The overall rate of malignancy for B3 lesions after excision was 21%. The B3 lesion-specific rates of malignancy were 6% for radial scars, 14% for papillomas, 35% for AIEP, and 44% for lobular neoplasia. Of the patients with a B4 categorization, 90% (44 of 49) were diagnosed with carcinoma after surgery. Those that were "suspicious for ductal carcinoma-in-situ" and "suspicious for invasion" correlated accurately with excision findings in 81% and 89% of patients, respectively.

Conclusions: Management of lesions in the B3 categorization must be tailored to the patient because the specific lesion types are associated with highly variable rates of malignancy. A repeat biopsy or a therapeutic wide local excision should be undertaken in lesions with a B4 NCB categorization because such lesions are associated with a particularly high risk of malignancy at excision.

Key Words: Categorization • Excision histology • Malignancy • Needle core biopsy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
The B classification1 was proposed by the UK Breast screening program as a way of recognizing that between benign breast lesions (B2) and malignant lesions (B5) on needle core biopsy (NCB) lay a small group of lesions whose malignant potential could not be adequately ascertained by NCB alone (B3/B4). Worldwide, regardless of the classification system used, breast units readily identify with the heterogeneous group of lesions by NCB that are of "uncertain malignant potential." These lesions include atypical intraductal epithelial proliferations (AIEPs), lobular neoplasia (LN), papillary lesions, radial scars (RS), and potential phyllodes lesions. Their importance lies in the lack of clarity regarding optimal management of these lesions with ongoing fluctuations in trends of management or perceived associations with malignancy.

The adoption of a "borderline" or "suspicious for malignancy" (B4) category is not in widespread use but represents a potentially useful classification system. In practice, these lesions are less difficult to manage in that surgery is almost always required. The actual importance of these preoperative findings is unclear, however, leading to difficulties in counseling patients before surgery or planning the nature and extent of operations.

The aim of this study was to correlate B3 or B4 findings by NCB with excision histology to determine the corresponding rates of malignancy for the various lesions in these groups. We also sought to determine whether the use of a B4 category was highly correlated with malignancy to the extent that it could potentially affect the planning of treatment strategies.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Study Population
The study population was derived from all women who underwent NCB for evaluation of a breast abnormality at St Vincent’s University Hospital, Dublin, Ireland, and the Merrion Breast Screening Unit over a 6-year period from January 1999 to July 2005. Patients were identified from a database of clinical information relating to consecutive patients presenting to the breast symptomatic service and population based screening service at the hospital. The symptomatic clinic was attended by patients with breast abnormalities who were referred by their primary-care physicians. The screening population was derived from those women attending the Irish National Breast Screening Programme ("Breastcheck"), which offers two-view mammographic screening every 2 years to women aged 50 to 64 years. All patients in the study population underwent clinical examination and radiological investigation.

Image-Guided Biopsy
Ultrasound-guided biopsy was used for the evaluation of sonographically visible lesions and was performed with the patient in the supine or decubitus position with a high-resolution 12.5 MHz linear array transducer. A 14-gauge automated needle device with a 22-mm throw biopsy gun was used (Tru-Core, Medical Device Technology, Gainesville, FL). Three NCBs were retrieved in the case of ultrasound biopsies. The accuracy of a three-core retrieval policy has been validated in two previous studies.2,3 The principle indication for stereotactic-guided NCBs was for lesions not seen on ultrasound. Stereotactic-guided NCBs were performed with the patient in the upright position with a digital Siemens Optima machine (Solna, Sweden) and a spring-loaded biopsy device (Tru-Guide, Bard Ltd., Crawley, UK). Fourteen-gauge, and occasionally 11-gauge, needles were used for stereotactic NCBs during the study period. Our protocol was to retrieve eight cores under the stereotactic technique for each lesion, in line with international recommendations.4–6 Clinical NCBs were guided by palpation and were performed with a Pro-Mag biopsy gun (Manan Medical Products, Northbrook, IL) with a 14- or 16-gauge needle.

Pathological Assessment
NCBs were fixed in formalin, embedded in paraffin, and processed according to standard protocol. Each biopsy specimen was stained with hematoxylin and eosin and examined at a minimum of two levels. Samples were reported as normal/nondiagnostic (B1), benign (B2), uncertain malignant potential (B3), suspicious but not diagnostic of malignancy (B4), or malignant (B5) according to the nonoperative B classification system.1 In addition, B4 lesions were further categorized as "suspicious for ductal carcinoma-in-situ (DCIS )" or "suspicious for invasion."

The "uncertain for malignant potential" category included AIEP, RS, papilloma, LN (which includes atypical lobular hyperplasia and lobular carcinoma-in-situ), and potential phyllodes tumor. Rare lesions such as mucin were included under the heading of "miscellaneous." The term AIEP was used to describe intraductal or intralobular cellular proliferations showing cytological and/or architectural atypia. Depending on the degree of atypia and suspicion of DCIS, these lesions were categorized as B3 or B4. The term AIEP is considered preferable to the frequently used term atypical ductal hyperplasia (ADH). The latter is a diagnosis reserved for excision specimens when the abnormality has been fully examined and the diagnosis of DCIS excluded.

Combinations of lesions were also recorded (e.g., RS or papilloma with AIEP) and similarly categorized as B3 or B4, according to the degree of atypia. Phyllodes tumors were not considered to be malignant if they were considered benign or borderline at excision.

Follow-up
All NCB results were reviewed at a weekly multi-disciplinary meeting attended by specialist breast histopathologists, radiologists, surgeons, oncologists, and radiotherapists. At these meetings, recommendations were made to discharge, monitor clinically, further investigate, or refer for diagnostic or therapeutic surgery. Patients who underwent surgical excision were reviewed again at these meetings. For the purposes of this study, further follow-up information on the status of all patients who had a B3 or B4 lesion that did not undergo surgery was also retrieved.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Patient Population
In total, 3729 patients underwent NCB for breast abnormalities over the 6-year period. From this group, 262 (7%) were categorized as B3 or B4. A total of 131 (50%) were derived from the symptomatic service and 131 (50%) from the breast screening service. A total of 55% (n = 143) of these B3/B4 NCB were performed under ultrasound guidance, 34% (n = 90) under stereotactic guidance, and 11% (n = 29) under clinical guidance. The total open biopsy rate for B3/B4 lesions was 86% (226 of 262).

B3 Lesions
A total of 211 patients were diagnosed with B3 lesions by NCB, representing 5.5% of our total NCBs. The open biopsy rate after this finding was 84% (177 patients). The overall rate of malignancy for B3 lesions was 21% (37 of 177) after excision, or 18% (39 of 211) if all patients were considered. The lesion-specific rates of malignancy after excision were 6% for RS, 14% for papillomas, 35% for AIEP, and 44% for LN (Table 1Go). A B3 NCB suggesting the possibility of phyllodes tumor was associated with a 34% rate of phyllodes tumor at excision, but none of these tumors were malignant. However, 11% (4 of 35) of patients who had a potential phyllodes tumor by NCB had DCIS (n = 1), invasive disease (n = 2), or a sarcoma (n = 1) at excision.


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  		TABLE 1. Correlation of B3 needle core biopsy (NCB) findings with subsequent excision findings
 
The combined findings of AIEP and RS were associated with a 37% rate of malignancy at excision. Within the B3 category, if a papilloma was associated with the additional B3 findings of RS, AIEP or atypia within the papilloma the associated rate of malignancy was 35%. The radiologic features of those that had LN at excision are listed in Table 2Go. Only LN that was associated with suspicious radiology was found to have malignancy at excision.


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  		TABLE 2. Radiological features of patients with needle core biopsy finding of lobular neoplasia
 
B4 Lesions
Fifty-one patients had tumors that were assigned to the B4 category by NCB. The open biopsy rate after this finding was 96% (49 of 51). Of these, 90% (44 of 49) were diagnosed with carcinoma after surgery (Table 3Go). Tumors assigned a B4 categorization were further subcategorized as "suspicious for DCIS" (n = 27), "suspicious for invasion" (n = 21), or other (n = 3) on the basis of the NCB results. Of patients whose findings were "suspicious for DCIS," 81% (n = 22) had DCIS at excision, 4% (n = 1) had invasive disease, and 15% (n = 4) had ADH. Of the 21 patients who had B4 lesions "suspicious for invasion," two patients did not undergo surgery. Of those remaining (n = 19), all had carcinoma at excision, and 89% (17 of 19) had invasive disease.


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  		TABLE 3. Correlation of 51 B4 needle core biopsy (NCB) findings with subsequent excision findings
 
Nonoperative Management
Thirty-six patients did not have their lesions excised. Follow-up was attainable for 26 patients, with a median follow-up time of 29 months. Two patients with B3 lesions subsequently developed carcinoma. One of these patients with a diagnosis of "mucin" in NCB was diagnosed with mucinous carcinoma >2 years later. Another patient with a B3 diagnosis of AIEP was diagnosed with DCIS 4 years later. Two patients had B4 lesions that were not excised. One patient was diagnosed at the same time with carcinoma in the opposite breast and was treated medically. The other patient was elderly and unfit for surgery, and was treated with endocrine therapy.

If these patients were included in the analysis, the associated rates of malignancy was 5% for RS, 11% for papillomas, 28% for AIEP (B3), and 33% for LN (Table 1Go). The combined finding of RS and AIEP was associated with a 32% rate of malignancy and papillomas with atypia, AIEP, and/or RS was associated with a 29% rate of malignancy.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
Lesions of "uncertain malignant potential" (B3) by NCB encompass a spectrum of lesions, each associated with a risk of malignancy. In addition, combinations of these lesions by NCB are not infrequent, although it is uncertain whether risks of malignancy in these cases are cumulative. A second group of lesions exist that are known under some classification systems as B4 lesions.1 These cause more concern because they are considered lesions "suspicious for malignancy." Typically, they represent atypical findings by NCB, which lack the quantitative or qualitative criteria to permit a definitive diagnosis of carcinoma but cause sufficient concern to require early surgical excision. Whether this preoperative level of suspicion by NCB is justified is unclear. The lack of clarity regarding the significance of a B4 lesion in turn leads to difficulty in planning the extent of the surgical procedure or considering whether sentinel node biopsy may be appropriate in this patient population.

The heterogeneity of the first category of lesions, those "of uncertain malignant potential" (B3), is emphasized in this study, with associated rates of malignancy at excision ranging from 6% to 44%. This study has outlined the relative rates of malignancy associated with given lesions in a consecutive series of patients using similar techniques in a similar setting. It also provides information as to the outcome of the combination of these lesions by NCB compared with excision findings. This 6-year retrospective study was based on automated rather than vacuum-assisted biopsy techniques, which have only recently been introduced into our practice. However, we have previously reported high levels of accuracy, in particular with ultrasound-guided automated techniques,2,3 and therefore, we believe our results are representative of current practice.

Radial Scars
RS are rare, representing approximately .01% of all NCBs.7–9 The advent of screening programs means that they are increasingly being detected. Radiologically, they cannot be reliably distinguished from carcinoma. Whether excision should be mandatory has not yet been clarified. Earlier reports suggested a strong association of RS with carcinoma,10–14 but more recent studies concentrating on those diagnosed preoperatively by NCB report low associated malignancy rates of 0% to 8%.7,15–17 The rate is particularly low in those with only RS by NCB without associated findings such as atypia.16 In our series of 63 patients, the overall rate of malignancy after excision was 17%. However, in subgroup analysis, 6% of patients with RS only by NCB had malignancy at excision. However, when RS was seen in combination with AIEP or LN by NCB, the risk of malignancy at excision was 37%, no higher than the associated risk of malignancy attributed to AIEP or LN alone. Our results indicate that patients with RS only on NCB could potentially be monitored.

Papilloma
Contrary to the findings of Carder et al.,18 a B3 finding of papilloma was associated with carcinoma at excision. This occurred in 14% of patients whose papillomas were excised in our study. Determining the malignant potential of papillary lesion by NCB is difficult. The presence of a myoepithelial layer does not preclude malignancy, and diagnosis depends on features such as cellular atypia and cellular monotony.19 Our institutional policy has been to advise excision to all patients who are found to have papilloma by NCB. This has allowed us to have a higher correlation between NCB pathology and excision findings than many other studies,20,21 which may only remove high-risk lesions.22 Traditionally, most studies have suggested that benign papillomas by NCB should not be excised21 owing to a low associated malignancy rate.19,21–23 The high associated rate of malignancy in the present study as well as a high associated rate of ADH suggests that surgical intervention is warranted in most of these patients. In addition, if the B3 papilloma was associated with atypia or with additional findings by NCB that in themselves still merited a B3 status, the risk of malignancy was as high as 29%. Overall, if all papillomas including B4 papillomas are analyzed, the associated rate of malignancy was 26%.

Lobular Neoplasia
Lobular neoplasia is a term used to encompass a spectrum of lesions, including lobular carcinoma-in-situ and atypical lobular hyperplasia. LN, unlike AIEP, is not universally excised. Studies on LN are limited by the rarity of this lesion24,25 and the fact that in these studies, many of these lesions were not excised.26 The management of LN is particularly controversial. This lesion tends to be multicentric27 and carries a risk of both ductal and lobular invasive carcinoma in the contralateral as well as ipsilateral breast.25,27,28 LN is typically invisible on mammography, leading to arguments29 that the finding of LN on core NCB biopsy (which may be incidental) is less important than the level of suspicion raised by the nature of the mammographic lesion associated with it. Subsequently, the findings of carcinoma at excision may be related to a selection bias in removing lesions that have preoperative features other than LN that are a cause of concern.

Against this, increasing numbers of studies are recommending routine excision of these lesions because LN by NCB is found to be associated with high rates of malignancy at excision.24,26,30 Arpino et al.,26 in a review of the literature, found that of those that were excised, there was an average of 16% rate of carcinoma (range, 6%–53%) associated with atypical lobular hyperplasia and 26% (range, 15%–50%) rate of carcinoma associated with lobular carcinoma-in-situ. In the present study, 44% of all lesions with LN that were excised were found to have associated carcinoma. However, those that were associated with malignancy were also associated with suspicious imaging findings (BIRAD 4 or 5) (Table 2Go), whereas those that had no malignancy at excision or at follow-up were associated with relatively nonsuspicious radiology such as indeterminate calcification. Although analysis is limited by the rarity of the lesion (.3% of all our NCBs), our findings would support a policy of offering surgical excision to all patients with LN by NCB who have associated suspicious radiology, but do not necessarily support excising all LN lesions.

Phyllodes Tumors
There have been few reports on the predictive value of NCBs, which are equivocal for phyllodes tumor.31–33 We have previously demonstrated the great difficulty in definitively diagnosing phyllodes tumor by NCB before surgery, and we have shown that most preoperative NCBs in these patients are equivocal.33 In the present study, a NCB of this nature was associated with a 34% rate of phyllodes tumor at excision and, unexpectedly, a high rate of associated carcinoma or sarcoma. The associated high rate of carcinoma is difficult to explain. In one patient, the foci of invasive lobular carcinoma was minute (1.5 mm), and in another, the finding was that of low-grade DCIS, suggesting that the finding of carcinoma may have been incidental. However, these results, in conjunction with our high rate of phyllodes at excision, reinforce the importance of a policy of early excision of all such lesions.

Atypical Intraductal Epithelial Proliferation
The traditional atypical ductal hyperplasia category has been problematic in the past,34–37 representing a spectrum from mild atypical changes to low grade DCIS. More recently, the World Health Organization has tried to address this by bringing in the ductal intraepithelial neoplasia (DIN) classification38 whereby flat epithelial atypia whose risk of malignant transformation is currently unknown39 is designated DIN 1A, atypical ductal hyperplasia as DIN 1B, and low grade DCIS as DIN 1C. DIN 2 is then reserved for grade 2 DCIS. However, this classification system has not been widely accepted and has some vigorous opponents, particularly those who argue that there is no direct evidence that atypical hyperplasia is a precursor to breast carcinoma.40

In the B classification, AIEP can be categorized as mild/moderate (B3) or suspicious for malignancy (B4). These categories recognize that those lesions found by NCB to have a minor or moderate degree of atypia, frequently architectural, should be distinguished from severe atypia, suspicious for DCIS. In the later category, AIEP (B4) is diagnosed because it has some, but not all, of the features of DCIS. NCB specimens are limited by the amount of tissue available, which may result in the qualitative changes of DCIS being represented, but insufficient quantity of change for a definitive diagnosis.

In addition to AIEP suspicious for DCIS, the B4 categorization also includes atypical glandular cells or single cells suspicious for invasion. Small foci of invasive carcinoma insufficient for immunocytochemical studies, or neoplastic cells on the outer aspect of a sample may result in a B4 categorization. Technical problems such as crushed or poorly fixed NCBs may also preclude a definitive diagnosis and lead to either a B4 or B1 (inadequate) categorization.

In the present study, AIEP lesions placed into the B3 category have a 35% associated rate of carcinoma. In the literature, up to 40% of all AIEP lesions are upgraded to either DCIS or invasive cancer.41–46 This study has also demonstrated that when AIEP is seen in combination with other B3 lesions, it seems to bring the association with carcinoma up to at least this level. These results emphasize that of all the B3 categories, this lesion in particular should be excised for full evaluation. With respect to the B4 categorization, 90% of patients who had AIEP (B4) were found at excision to have carcinoma. Of the B4 lesions suspicious for DCIS, 82% had a diagnosis of DCIS at excision, and a further 4% had invasive disease, whereas those B4 lesions suspicious for invasion resulted in an 89% rate of invasive carcinoma at excision.

B4 Category
The present study has demonstrated that the "suspicious for malignancy" B4 classification is of considerable value in the potential management of surgical patients. Patients who have B4 lesions have a 90% risk of carcinoma at excision, which is similar to the findings of Lee et al.47 The results of this study suggest that in these patients, a repeat NCB should be performed to gain a definitive preoperative diagnosis. Failing this, an attempt at wider margins rather than diagnostic excision should be considered preoperatively in those patients undergoing breast-conserving surgery. In addition, this study also has demonstrated that lesions that were suspicious for malignancy could be subcategorized into two groups on the basis of their NCB results. They were either AIEP suspicious for DCIS, or lesions suspicious for invasion. Of particular interest was the finding that a very high correlation existed between the excision biopsy findings and the NCB pathology in this regard. Eighty-two percent of patients who had lesions that were suspicious for DCIS had DCIS at excision, and 89% of those with lesions suspicious for invasive disease had invasive disease at excision. Consequently, these results seem to justify offering sentinel node procedures to the latter group.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
The results of this study demonstrate the value of segregating indeterminate lesions into those of "uncertain malignant potential" and those "suspicious for malignancy," which have a 21% and 90% rate of malignancy at excision, respectively. In the first group, we emphasize that lesions of "uncertain malignant potential" (B3) are a heterogeneous group of lesions, with varying malignant potential. Within this group, we would recommend that papillomas that have high rates of malignancy at excision (14%) should be excised, that LN in association with suspicious radiology should be excised, but that RS alone with a 6% associated rate of malignancy could potentially be managed conservatively. Most combined lesions, particularly if atypia is present, warrant excision. We have also demonstrated the value of a B4 classification in the surgical management of breast carcinoma, which correlates with a 90% rate of malignancy at excision. Moreover, within this group, two definite classes emerge, each with a very high correlation with in situ or invasive disease at excision. The results of this study suggest that repeat NCB or an attempt at obtaining wider margins is justified in patients with B4 NCB biopsy findings and that sentinel node biopsy is warranted in those patients with NCBs "suspicious for invasion."

Received for publication July 22, 2006. Accepted for publication July 27, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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