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Review |
1 Department of Radiology, Indiana University School of Medicine, Indiana University Hospital, Rm. 0279, 550 N. University Blvd., Indianapolis, IN 46202
Received August 23, 1999;
accepted after revision October 4, 1999.
Address correspondence to H. E. Reynolds.
Introduction
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One hundred seventy-three of the 472 titles composing search 1 were eliminated because of lack of relevance to the subject of breast core needle or vacuum-assisted biopsy. Thirty-six of these 173 were fine-needle aspiration papers. Of the remaining 299 citations, 293 articles were obtained and reviewed for relevance. Six articles could not be obtained at this institution's medical library or via interlibrary loan. Each of the remaining 293 articles was meticulously reviewed for the presence of core needle and correlative surgical excisional biopsy data on any of the following seven benign breast conditions: atypical ductal hyperplasia (ADH), atypical lobular hyperplasia, radial scar, lobular carcinoma in situ (LCIS), benign papillary lesions, benign phyllodes tumor, and pseudoangiomatous stromal hyperplasia. Two hundred twenty-six articles that did not contain specific correlated information on these conditions were deemed irrelevant. The remaining 67 [2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68] form the basis of this report.
Care was taken to avoid data duplication. One multiinstitutional report [23] included previously published data on ADH from three other institutions [34,41,60]. In this case, only the data in the multi-institutional paper were included in the analysis. Several reports from a particular institution were built on previously published data from the same institution. Therefore, the reporting periods were carefully analyzed to determine if any overlap existed. If the results in the earlier reports were included in the later reports, only the later results were included in the analysis (Table 1). In one case, an earlier report [43] contained more references to the lesion of interest (papilloma) than a later report from the same institution [16] (Table 1). Therefore, the data from the earlier report were used.
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Diseases reported as "atypical ductal hyperplasia" (n = 434), "atypical hyperplasia" (n = 132), "atypia" (n = 45), "atypical ductal hyperplasia versus atypical lobular hyperplasia" (n = 12), "atypical ductal hyperplasia or lobular carcinoma in situ" reported together (one paper in which the authors did not separate atypical ductal hyperplasia cases from LCIS cases) (n = 6), and "fibroadenoma with atypical ductal hyperplasia" (n = 1) were grouped together as ADH (n = 630) for the purposes of this analysis.
"Papilloma" (n = 15) or "benign papillary lesion" (n = 9) were grouped together as "low-suspicion papillary lesions" (n = 24). "Papillomatosis" (n =2), "papillary lesion with atypical ductal hyperplasia" (n = 10), and "papilloma with atypia" (n = 1) were grouped together as "high-suspicion papillary lesions" (n = 13). Lesions reported as "sclerosing papilloma" (n = 2) were considered separately.
"Phyllodes tumor" (n = 4) and "cellular fibroadenoma versus phyllodes tumor" (n = 5) were grouped together as "phyllodes tumor" (n = 9).
"Atypical ductal hyperplasia versus ductal carcinoma in situ" (n = 4), "atypical ductal hyperplasia versus cribriform carcinoma" (n = 1), "atypical lobular hyperplasia with possible invasive lobular carcinoma" (n = 1), "mass with atypical features" (n = 7), and "calcifications with atypical features" (n = 6) were excluded from this analysis.
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Of the 630 ADH lesions, 403 were biopsied with an automated spring-loaded gun and a 14-gauge needle using either sonography or stereotaxis for guidance. Of the 375 with surgical correlation, malignancy was discovered in 155 (41%). The eight patients who were followed up for 24-31 months without malignancy diagnoses were a part of this group. Including them makes the malignancy rate for this biopsy method 155 (40%) of 383. One hundred twelve of the 630 ADH lesions were biopsied with a 14- or 11-gauge directional vacuum-assisted device. Of the 98 with surgical correlation, malignancy was found in 15 (15%). Thirty-six ADH lesions were biopsied with either a 14-gauge automated gun or a 14-gauge vacuum-assisted device. In the 32 of these lesions with surgical correlation, malignancy was discovered in 17 (53%). Fifteen ADH lesions were biopsied with a spring-loaded automated gun and a 14- or 15-gauge needle. At surgery, four (27%) of 15 lesions revealed malignancy. Twenty-three ADH lesions were biopsied with a spring-loaded automated gun and an 18- or 20-gauge needle. All 23 lesions had surgical correlation, and malignancy was found in 13 (57%). Nine ADH lesions were biopsied with a 15-gauge nonautomatic system with stereotactic guidance; six (67%) of nine lesions revealed malignancy at surgery. Eighteen ADH lesions were palpable abnormalities biopsied with an 18-gauge nonautomatic core needle system with no imaging guidance. All were surgically excised and one malignancy (5.5%) was found. Fourteen ADH lesions were biopsied with devices not specified by the authors. Of the nine lesions with surgical correlation, malignancy was found in three (33%).
LCIS and Atypical Lobular Hyperplasia
LCIS was reported in four (0.02%) of 18,542 needle biopsies. After all four
were excised, malignancy was found in two lesions (50%). One lesion was
identified as ductal carcinoma in situ; the other was identified as invasive
ductal carcinoma. Ten atypical lobular hyperplasia lesions (0.05%) were
reported among the 18,542 biopsies. Of the nine lesions with surgical
correlation, an invasive lobular carcinoma was found in one (11%).
Papillary Lesions
Among the 18,542 biopsies, 29 papillary lesions (0.16%) were reported.
Among these 29 lesions were 24 low-suspicion papillary lesions, 13
high-suspicion papillary lesions, and two sclerosing papillomas. Of the 20
low-suspicion papillary lesions with surgical correlation, no malignancies
were identified. In addition, three of the 24 low-suspicion papillary lesions
had mammographic follow-up for at least 36 months with no malignancies
discovered for a malignancy rate of 0 of 23. All 13 high-suspicion papillary
lesions were surgically excised, revealing malignancy in five lesions (38%).
Four of the malignancies were diagnosed as ductal carcinoma in situ; the fifth
malignancy was diagnosed as a tubular carcinoma. Both of the sclerosing
papillomas were excised. Ductal carcinoma in situ was discovered in one lesion
(50%).
Phyllodes Tumor
Nine benign phyllodes tumors (0.05%) were reported among the 18,542 needle
biopsies. Of the seven lesions with surgical correlation, one (14%) was
malignant (malignant phyllodes tumor).
Radial Scar
Radial scar lesions were reported in 18 (0.1%) of 18,542 needle biopsies.
Of the 15 lesions surgically excised, ductal carcinoma in situ was discovered
in one (6.7%). This lesion was biopsied with a spring-loaded automated gun and
a 14-gauge core needle.
Pseudoangiomatous Stromal Hyperplasia
Nine cases (0.05%) of pseudoangiomatous stromal hyperplasia were reported
among the 18,542 needle biopsies. Of six with surgical correlation, no
malignancies were found. Two lesions had imaging follow-up at 6 months that
showed stability.
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Early in the evolution of breast core needle biopsy, the diagnosis of ADH by core needle biopsy was found to be unreliable. The initial technique of using a 14-gauge needle with an automated spring-activated biopsy gun resulted in a 50% rate of disease underestimation [57,60] (rate at which malignancy is found when a core needle biopsy-diagnosed ADH lesion is surgically excised). Disease underestimation is likely related to sampling error, which in turn is related to the volume of tissue removed at biopsy. With the advent of the vacuum-assisted biopsy device, now widely in use, much larger volumes of tissue are being removed at needle biopsy than was previously possible. With the 14-gauge needle and automated-gun technique, individual specimens weigh, on average, around 17 mg compared with 36 mg for the 14-gauge vacuum-assisted device and 94 mg for the 11-gauge vacuum-assisted device [72]. In this literature review, use of the 14-gauge needle and automated-gun technique resulted in an underestimation rate of 41% compared with a rate of 15% when the vacuum-assisted technique was used with either 14- or 11-gauge probes. Though this figure represents a major technical improvement, the rate is unacceptably high, and it is recommended that patients with ADH diagnosed percutaneously, regardless of the technique, undergo surgical excision.
LCIS and Atypical Lobular Hyperplasia
Foote and Stewart [73]
first recognized LCIS as a distinct entity in 1941. They described a lesion
consisting of a proliferation of large cells with proportionally large clear
nuclei in lobules that are normal in size or even slightly small. LCIS is a
benign highrisk marker that is frequently bilateral. Affected patients have a
30% lifetime risk of developing invasive carcinoma of either breast. The
lesion has no clinical or mammographic manifestations and is essentially
incidentally diagnosed after biopsy for some other reason. An important
feature of LCIS mentioned in Foote and Stewart's report is its tendency to
coexist with other forms of carcinoma, including comedocarcinoma, ordinary
invasive ductal carcinoma, and tubular carcinoma.
Because LCIS typically has no mammographic manifestations, it is rarely encountered as the sole histologic diagnosis after core needle breast biopsy. In this literature review, four cases were identified, two (50%) of which were found to harbor malignancy at excision. Both carcinomas were of ductal origin. There are two reasons it might be reasonable to recommend surgical excision after a core needle biopsy yielding LCIS alone (no other disorders seen). First, LCIS is usually mammographically occult. Thus, the mammographic lesion that prompted the biopsy may correctly still be considered undiagnosed. LCIS was an incidental finding in the vicinity of the mammographic lesion. The second reason is that breast malignancy, whether of ductal or lobular origin, is frequently found to have areas of LCIS nearby. Thus, a core needle biopsy diagnosis of LCIS alone may represent a sampling-error problem similar to that seen with ADH. Clearly, insufficient data in the literature exist for firm treatment recommendations at this time.
Likewise, experts differ on what precise criteria should be used to distinguish atypical lobular hyperplasia from LCIS. Again qualitatively when some, but not all, of the criteria for LCIS are present, atypical lobular hyperplasia is usually diagnosed. However, if all the criteria for LCIS are present, atypical lobular hyperplasia may also be diagnosed if less than one half [74] or less than three fourths [75] of the acini in a terminal ductal lobular unit are involved. Atypical lobular hyperplasia is a much less common condition than ADH. In this literature review, 10 cases of atypical lobular hyperplasia were identified. Of the nine with surgical correlation, one lesion (11%), an invasive lobular carcinoma, was malignant. As with ADH, disease underestimation is a risk with atypical lobular hyperplasia.
Papillary Lesions
There are several varieties of papillary lesions of the breast. The most
common is the solitary central intraductal papilloma, which is a benign tumor
arising from the epithelium of a major duct in the subareolar region. It
contains a well-defined fibrovascular core and the usual two populations of
cells, although the myoepithelium is inconsistent
[76]. These lesions frequently
undergo hemorrhagic infarction, resulting in a bloody nipple discharge.
Peripheral papillomas originate in a terminal ductal lobular unit and extend
along small ducts [77]. They
are often multiple and associated with various degrees of hyperplasia of the
usual and atypical varieties. Thus, these papillomas are associated with an
increased risk of subsequent malignancy, whereas the central papillomas are
not. Page and Anderson [78]
have stated that any risk of malignancy associated with these lesions
"can be assessed from the degree of atypical pattern or cytology present
within [them]." Sclerosing papillomas are benign papillary lesions that
have undergone extensive sclerosis and hyalinization
[79]. Microscopically, they
can mimic radial scar lesions or even invasive carcinoma
[79]. Finally, the term
"papillomatosis" deserves some attention. Different experts
unfortunately define this term in different ways. Tavassoli
[80] states that
papillomatosis is "also referred to as multiple papillomas,"
whereas Page and Anderson [81]
and Rosen [82] indicate that
the term is commonly used by pathologists interchangeably with ductal
hyperplasia, even though this usage is discouraged. Therefore, in common
usage, the term "papillomatosis" may not refer to a papillary
lesion at all but rather to an entity along the spectrum of ductal
hyperplasia.
In this literature review, 24 papillomas or benign papillary lesions were identified. No malignancies were discovered among 20 papillomas with surgical correlation or among the three with mammographic follow-up for at least 3 years. Thus, excision can be avoided with papillomas diagnosed at core needle biopsy if no worrisome histologic features are present. If the papillary lesion displays cytologic atypia or frank ADH or if the diagnosis is papillomatosis, disease underestimation risk is high. In this literature review, five (38%) of 13 such lesions were found to harbor malignancy at surgical excision. Two cases of sclerosing papilloma were identified, one of which contained ductal carcinoma in situ at excision.
Phyllodes Tumor
Phyllodes tumor, also known as cystosarcoma phyllodes, is a fibroepithelial
tumor related to fibroadenoma. These tumors typically present as large
palpable masses and are most common in the fifth decade of life. They are
commonly classified histologically as benign, low grade (or borderline), or
malignant [83]. Malignant
phyllodes tumors display malignant cytologic features in the stroma. Page and
Anderson [84] stated,
"...recognition of malignancy depends on thoroughly sampling...[these]
lesions." The core needle biopsy may thus be susceptible to sampling
error in the assessment of these lesions. Of the seven "benign"
phyllodes tumors with surgical correlation identified in this review, one was
malignant (malignant phyllodes).
Radial Scar
Radial scar (radial sclerosing lesion) is an uncommon but important
disorder. The importance of this lesion is twofold. First, having a spiculated
appearance, it is a known mimicker of carcinoma on mammography. Furthermore,
on gross pathologic inspection, a spiculated lesion with a firm fibrous center
that is frequently puckered is the usual pattern that may be impossible to
distinguish from carcinoma
[85]. Second, it has a known
association with carcinoma. In a review of 126 radial scar lesions, Sloane and
Mayers [86] found carcinoma in
22 of the lesions (17%). Sloane and Mayers included three cases of LCIS with
their carcinoma patients. Excluding these three cases, they found ductal
carcinoma in situ or invasive carcinoma in 19 lesions (15%). Curiously, this
relationship was dependent on the size of the lesion, the age of the patient,
and the method by which the radial scar was detected. No malignancies were
detected in radial scars of less than 6 mm in diameter, and similarly, no
malignancies were detected in patients younger than 40 years old. The
incidence of carcinoma in radial scars was 43% detected as a mammographic
abnormality, 22% detected as a palpable mass, and 1.2% detected as an
incidental finding at histology after biopsy for some other condition.
For this reason, it has generally been advised that radial scar lesions diagnosed at core needle biopsy be excised. In fact, if the mammographic appearance of the abnormality indicates that radial scar is likely, excision may be a more appropriate approach than percutaneous biopsy. In this review, 18 radial scar lesions were identified. Of the 15 lesions that were surgically excised, malignancy (ductal carcinoma in situ) was discovered in one (6.7%).
Pseudoangiomatous Stromal Hyperplasia
Pseudoangiomatous stromal hyperplasia is an uncommon tumor that is
significant because it can be mistaken for angiosarcoma at histology
[87,88].
Only nine core needle biopsy-diagnosed cases of pseudoangiomatous stromal
hyperplasia were identified. In six with surgical correlation, no malignancies
were discovered.
Study Limitations
This literature review has several weaknesses. First, the technique of
breast core needle biopsy has evolved significantly since its inception. Thus,
combining results from studies published over an 18-year period necessarily
involves pooling data from studies in which the biopsies were performed with
different techniques. In many reports, the biopsy technique even varied over
the course of the reporting period. Thus, what has been done here, though
necessary, is somewhat like combining apples and oranges to make more apples
or more oranges. This inconsistency may limit the validity of these results. A
second limitation is that in the core needle biopsy literature, histologic
results have not been reported in a standardized fashion. For example, in the
case of atypical hyperplasia, among other designations, lesions have been
reported as atypia, atypical hyperplasia, ADH, and ADH versus atypical lobular
hyperplasia. An attempt was made to organize this varied terminology so that
results of similar histologic entities could be compared; however, the method
used is clearly imperfect and subject to criticism. A third limitation is the
issue of data duplication. A dedicated effort was made to avoid this pitfall;
however, it was not always possible to identify overlapping data in reviewing
multiple reports from the same institution, especially if the focus of each
report was different.
Conclusion
Despite these weaknesses, these results give a more complete picture of the
reliability of breast core needle biopsy in making certain uncommon benign
diagnoses. However, for some of these conditions insufficient data were found
to give clear guidance in patient treatment after biopsy. Given current
knowledge, I recommend surgical excision after a core needle biopsy diagnosis
of ADH, atypical lobular hyperplasia, LCIS, high-suspicion papillary lesion,
sclerosing papilloma, radial scar, or phyllodes tumor. Low-suspicion papillary
lesions and pseudoangiomatous stromal hyperplasia may be safely observed.
Additional large multiinstitutional studies are urgently needed to accumulate
sufficient data on these uncommon benign entities.
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