Breast Mark A. Helvie, Bernard Naylor,
MD MB,
David E. Baker, MD2 Dorit ChB #{149} Kenneth A. Buckwalter, #{149}
Radiographically of Nonpalpable
S
the
use of mammography
pands,
terms:
Radiology
Breast, biopsy, 00.12985 00.81 e Breast neoplasms, #{149}Breast neoplasms, localization,
1990;
#{149} Ingvar
#{149} Breast,
diagno-
174:657-661
the
Andersson,
lesions
prove
to be
at time
of biopsy (1), methods to improve preoperative diagnostic characterization of such lesions would be helpful. Fine-needle aspiration (FNA) is commonly used to evaluate palpable breast lesions (2-8). In recent years, there have been reports of cytologic evaluation of nonpalpable lesions (916). The purpose of this study is to report our experience with and determine the efficacy of radiographically guided fine-needle aspiration (X-FNA) of nonpalpable breast le-
(500T; lumbia,
AND
breast
lesions
patients.
These
lesions
masses
clustered six
the
in 207 consecutive consisted of 142
or densities (66%), 67 groups of microcalcifications (31%), and
densities associated with calcifications all detected at mammography. Their were
smaller
as follows:
than
procedure,
coordinates
5-
10 mm, 94 (44%) were 11-20 mm, and 45 (21%) were greater than 20 mm. On the basis of their mammographic appearance, were classified into of suspicion: probably
lesions levels
low suspicion
for malignancy
mediate-to-high
suspicion
one of four benign
(A),
(B), interfor malignancy
possible based on the original mammographic report. When this was not possible, a mammographer (D.E.B.) rendered an opinion retrospecthis
subjective
(D). When
classification
was
tively. The decision to perform X-FNA (vs mammographic follow-up or surgical bi-
opsy) grapher.
was made During
by the original this
as many low-suspicion lowed up solely with patients
who
underwent
ly had more-suspicious history.
period,
mammoabout
X-FNA
Co-
usually
5-10
minutes
(Fig-
of the Depth
lesion
were
transferred
skin by means of ink was estimated as a fraction of the compressed breast
an orthogonal
view
(18).
The
needle
tipped
needles
2.5 or 3.5 cm long,
syringe
and
syringe
holder.
Solid
with
a
avail-
commercially
lesions
were
aspirated four times (16,19). If a cyst was encountered, we drained it as completely as possible with a 5-mL glass usually
syringe
and,
if possible,
obtained
a pneu-
mocystogram. The cytologic smears were prepared by expelling the aspirate onto the center of a glass slide and spreading it with the needie tip, beveled side down, in a longitudinal and crisscross manner for about 5-10 seconds. The smear was then fixed with a commercially available spray fixative before drying. In the cytopathology laboratory, the smears were stained by means of the Papanicolaou method. On the basis of the initial cytologic re-
twice
lesions were mammography. lesions
USA,
20-mL
able
(4%)
Eight
5 mm, 68 (31%) were
CGR,
ure). Most lesions were aspirated with the breast compressed craniocaudally, although medial or lateral approaches were used for some inferior lesions. The breast was compressed so that the lesion to be aspirated was positioned within the fenestration, and an initial radiograph was obtained (Figure, b). The
from
(3%), were
dedicated equipment
was inserted to the appropriate depth perpendicular to the skin (if near center beam), and the position of the needle over the lesion was documented with a repeat radiograph during initial aspiration (Figure, c). We used 22-gauge bevel-
Between May 1984 and September 1986, we performed X-FNA in 215 nonpalpable
with
with a fenestrated grid compression plate. (A few of the earliest aspirations were performed with a Mamex DC Mag unit, [Technomed USA, Bayshore, NY] similarly equipped.) The technique was similar to that described by Novak (17). The sitting patient was positioned for aspiration with the breast on the compression plate for the duration of
of the height
METHODS
X-FNA
General Electric Md) equipped
marks.
MATERIALS
.
mammographic
to the patient’s
sions.
(C), and malignant 1 From the Departments of Radiology (M.A.H., D.E.B., D.D.A., l.A., K.A.B.) and Pathology (B.N.), University of Michigan Hospitals, 1500 E Medical Center Dr, Taubman 2910, Box 0326, Ann Arbor, MI 48109-0325. From the 1989 RSNA annual meeting. Received May 4, 1989; revision requested July 1 1; revision received September 12; accepted September 15. Address reprint requests to M.A.H. 2 Current address: St Joseph Mercy Hospital, Ann Arbor, Mich. 3 Current address: Malmo General Hospital, University of Lund, Malmo, Sweden. C RSNA, 1990
We performed screen-film
of mam-
malignant
MD3
Aspiration
ex-
evaluation
mographically detected nonpalpable breast lesions has become an increasing clinical problem. Since only 15%30% of nonpalpable mammographic
diameters
calcification, sis, 00.3 00.125.
MD
Guided Fine-Needle Breast Lesions’
Radiographically guided fine-needle aspiration (X-FNA) in 215 nonpalpable, mammographically detected breast lesions was performed by means of a coordinate-grid localization system. Aspirates were categorized either into four cytologic groups or as simple cysts. Based on the most stringent cytologic criteria, the maximum sensitivity for detection of carcinoma was 97% and the specificity was 94%. However, according to these strict cytologic ciiteria, only 46% of aspirates contamed representative material. Based on less stringent cytologic cmiteria, the maximum sensitivity was 68% and the specificity was 97%. Forty-one of 74 lesions proved to be malignant at biopsy. Thirty-four patients did not complete adequate mammographic follow-up. High sensitivity and specificity can be achieved with X-FNA. However, management decisions ultimately require integration of mammographic findings with cytologic resuits. Close cooperation among mammographer, surgeon, cytopathologist, and patient is mandatory for successful results. Index
D. Adler, MD
#{149}
Imaging
folThe
general-
or clinical
Abbreviations: FNA X-FNA = radiographically
fine-needle guided
aspiration, fine-needle
aspiration. 657
ports,
we
lowing sis
grouped
four
for
our
Group
management This
al as well urn.
These
ing
and/or
This
group
mammary
epitheli-
grouped
breast
derived
from
turn
lymph
nodes,
fat
scar.
atypia or for malignancy. 4. Cytologic findings
findings of malig-
If typical nonbloody cyst fluid was tamed and the aspirated lesion disappeared or the pneumocystogram was
the fluid
tologic
was usually
evaluation
considered Surgical patients
and
a simple biopsy with
obnor-
not sent for cy-
the
lesion
was
cyst. was
recommended
suspicious
to
cytologic
find-
ings or findings indicating malignancy (groups 3, 4). Additionally, surgical biopsy was recommended for patients with suspicious
spite 2).
mammographic
benign Because
were
findings
cytologic different
involved
findings examination
which graphic with
generally suspicion. benign
of
paralleled the mammoLow-suspicion lesions
cytologic
findings
done despite the cytologic graphic findings. X-FNA surgical biopsies occurred times,
requiring
procedure. surgical
1,
variation
were
ally followed up mammographically. However, if biopsy was requested referring physician or patient,
biopsy
were
terval
mammography
breast
at 4 and
Table
up
of the
12 months
for with
cysts)
lesions
(54%),
Lesion
Table 1 Results of X-FNA Cy tology and Surgical Biopsy
(n
215) No.
Cytologic Benign
No. of Surgical Biopsies
Results
of
Cancers Found at Biopsy*
nonspecific (group 1) (n116)
36
12(33)
6
1(17)
8
4(50)
Benign
specific (group 2) (n30) Atypical or suspicious (group 3) (n8)
Malignant (group (n24)
cytologic
Type
Simple
4) 24
24(100)
cyst
0
(is=37)
Total
0(0)
74 (34)1
Percentages t Percentage rentheses. A
versus
Results
Cytologic
Results
Simple Cyst
or density (n 142) Microcalcifications Mass
at any
in the case of some
cytologic
41 (55)
of cancer in parentheses. of total X-FNA cytologies
in pa-
of Cytology (n
and Surgical
Benign (Groups 1, 2)
Biopsy
215)
Malignant (Groups 3, 4)
Results
74)
(ii
Benign
Malignant
36
85
21
13
22
0
57
10
17
17
1
4
1
3
2
37
146
32
33
41
(n67)
(or rea-
spiration
benign
2
X-FNA
biopsy
me-
Mass
in-
of these
surgical
not
Biopsy
and yearly thereafter. If progressive mammographic changes occurred intervals,
did
examination.
Mammographic Type
involved
after
215
Mammographic
localization
not referred followed
Alwas
were benign but nonspecific (group 1). Thirty-eight of 215 aspirates (18%) contained scant cellular material. There were 30 specific benign diagnoses (group 2) and 32 cytologic diagnoses of atypia or malig-
and mammoand subsequent at separate
a second
All patients
had
were
usuby the was
this
26 lesions
a
results
de-
mammographers
in the
follow-up
Thus, in 111
findings (groups 1, 2). In addition, 23 of the 26 (88%) had low-suspicion mammograms (classes A, B). Eight additional patients with benign cytologic findings returned for an initial follow-up study that demonstrated stability of their lesions, but they did not return for subsequent examinations. The 70 remaining patients have been followed up with mammography that showed stable findings for 9-48 months (median, 24 months). The X-FNA results for the 215 lesions are presented in Tables 1-3. In 1 16 of the
(groups
these patients, there was some in surgical biopsy recommendations,
to be simple
26 patients
for the
All
fibrocystic
nancy.
mal,
proved
recommended,
tissue).
3. Cellular
Group
lesions
in 74 of in 41 histoThirty-
cysts at the time of aspiration. definite diagnosis was made lesions (52%). The remaining 104 lesions followed up mammographically. though interval mammography
togeth-
fibroadenoma,
intramammary or radial
suspicious
seven
benign diagnosis. cytologic findings
included
with
Group
blood,
epithelium
normal
consistent
materi-
contained
were
2. Specific
disease, necrosis,
aspirates
nancy (groups 3, 4). The results in groups 3 and 4 were combined because surgical biopsy is recommended in all such patients. Forty-one cancers were discovered at surgical biopsy (Table 4). Twelve (29%) were noninvasive ductal carcinomas, and 29 (71%) were invasive carcinomas (one of which had an additional focus of lobular carcinoma in situ). Eleven of 12 cases (92%) of non-
RESULTS Surgical biopsy performed 215 lesions (34%) resulted logically proved carcinomas.
may result from madeof the mammographically (eg, the cytologic find-
of mammary Group
ba-
sample
that
aspirates
adjacent
fol-
the
included
as those
er because both quate sampling seen abnormality
the
are
“nonspecific”
inadequate
tissue,
into
decisions: but
group
contained
adipose
results which
1. Benign
findings. that
the
categories,
and microcalcifications
(n6) Total
was
recommended.
Table 3 Mammographic
Lesion
Class
versus
R esults
of Cytology Cytologic
and Surgical Results
(n
Biopsy 215) Histologic
Mammographic
658
Class
Simple Cyst
A(n=68) B(n95) C(n34) D(n18)
21 15 1 0
Total
37
Radiology
#{149}
Group 1 33 61 18 4 116
Results
(n
74)
Group 2
Group 3
Group 4
Malignant
Benign
13 13 4 0
1 3 4 0
0 3 7 14
0 7 19 15
3 16 12 2
30
8
24
41
33
March
1990
cancer were seen at as calcifications only. Twenty-eight (68%) of the cancers had positive (n 24) or suspicious (n = 4) cytologic findings. Of the 13 cancers with false-negative cytologic findings, 12 were in group 1. One patient in group 2 with a specific benign diagnosis (fibroadenoma)
ings were positive (groups 3, 4) (Table5). Note that positive cytologic findings were obtained in 18 of 22 carcinomas (82%) classified as masses or densities at mammography but in only nine of 17 carcinomas (55%)
proved
Nine patients (followed up mammographically after benign cytologic findings and low-suspicion mammograms) demonstrated progressive
invasive ductal mammography
at surgical
cancer. Nine with benign
biopsy
of thirteen cytologic
very
suspicious
ings
(classes
were
class
to have
lesions findings
(69%) had
mammographic
C, D). The B. Seven
find-
other
of the
four
41 cancers
had mammographic findings of low suspicion (class B). In three of these seven cancers, cytologic find(17%)
seen as microcalcifications (Table 4).
change Breast
of
these patients (classified in group 1). The first patient had a 50% increase in size of a benign-appearing 1-cm
Findings
versus
Cytology
at the
4-month
cinoma
with
nodes. This lumpectomy disease ment. mended
negative
had
a small
tions
and
mass
and
versus
patient,
because showed carcinoma.
Group
eventually
and
Group
1(n12)
2(nl) 3(n4) 4(n24)
Total
aspi-
mammobiopsy
and
Group 2
3 7 2
1 0 0
18 9 1
12
1
28
Classification
for 41
was
of Breast
1
3)
in
performed
irradiation
for 41 Cases
Mammograp Cytology
benign elected Surgical
of increasing calcifications, a minute focus of intraductal She was treated with
lumpectomy
16)
Mammographic
lymph
microcalcifica-
a nonspecific
rate; however, she graphic follow-up.
Total
Group
axillary
patient was treated with and irradiation and is
Cytology
Table 5 Cytology Carcinoma
exam-
free 29 months after treatBiopsy was initially recomto the second patient, who
Mammographic Findings Massordensity(n22) Microcalcifications (n Mass and microcalcifications(n
interval
ination; subsequent surgical biopsy demonstrated infiltrating ductal car-
this
on subsequent mammograms. cancer was proved in two
Table 4 Mammographic Carcinoma
nodule
Cases
3,4
of Breast
hic Classification
A
B
C
D
0 0 0 0
3 1 0 3
8 0 4 7
1 0 0 14
0
7
19
15
c.
(a) Coordinate-grid with the demonstrates
Volume
FNA
coordinate-grid that needle
174
Number
#{149}
technique compression (arrows)
3
is shown, plate is centered
with patient’s right breast in craniocaudal compression. (b) Preliminary radiograph demonstrates an 8-mm irregular mass (arrows). (c) Radiograph obtained after needle directly over the mass. This lesion proved to be invasive ductal carcinoma.
obtained placement
Radiology
659
#{149}
disease seven
free at 18 months. The patients with progressive
mammographic ment of nodules)
changes (ie, had benign
other
Table 6 Histologic
enlargefind-
carcinoma from the
detected ing
lesion),
cyst
that
was
in situ was mammogmaphically
one
had
Normal Fibrocystic Papilloma Radialscar
found
one
is a less
stringent
method
be-
cause it includes aspirates containing only blood, adipose cells, and/or mammary epithelial cells in the benign category. Calculated with this method, the maximum sensitivity and specificity for breast cancer detection by means of X-FNA are 68% and 97%, respectively. Method 2.-In this method it is recognized that mammary epithelium, blood, and/or adipose tissue may be derived from normal breast parenchyma adjacent to a specific lesion, and therefore benign results are mestricted to specific benign lesions (cytology group 2 and cysts). This much more stringent criterion results in an improvement of maximum sensitivity to 97%. The resulting specificity is 94%. However, this method eliminates many patients (54%). Additionally, a finding of mammary epithelial cells, blood, and/or adipose tissue may truly represent the mammographic “abnormality,” as might be the case in asymmetry of glandular 660
Radiology
#{149}
Group
change/fibroadenoma
Fat necrosis Atypical Scar
had
redevelopment of a previously aspirated cyst, and one had progressive growth of multiple bilateral breast nodules after starting estrogen therapy but refused further aspiration. These nodules were presumed to be benign and related to hormonal themapy. Although hemorrhage may occur at the time of X-FNA and manifest as a mammographic density, this was not a diagnostic problem in any patient at the 4-month follow-up examination. The data on the 33 patients who underwent biopsy and had benign histologic findings are presented in Table 6. Note that there were no false-positive (group 4) cytologic results. Four of these patients had group 3 cytologic results (atypical or suspicious). The accuracy of X-FNA can be determined with two different methods. In both calculations, the 34 lesions with follow-up of less than 9 months were deleted. Method 1.-One can divide all aspirate results into two groups: benign (cytology groups 1, 2 and cysts) and malignant (cytology groups 3, 4). This
Cytology
for 33 Benign
Lesions Cytology
an enlarg-
reaspirated,
versus
Histologic Result
ings. Three patients had histologic findings of fibmocystic change, one had a scar (although an incidental lobular distant
Results
ductal
hyperplasia
Total
breast
parenchyma
appearing
mammographic
The
evaluation mammogmaphic
mon
problem.
of a clinically oclesion is a com-
Currently
only
15%-
3
4
4 14 1 1 2 1 1
0 2 0 3 0 0 0
0 1 2 0 1 0 0
0 0 0 0 0 0 0
24
5
4
0
surgical
delay
30% of nonpalpable lesions seen at mammography will prove to be malignant at biopsy (1). Recent work suggests that with stricter mammographic criteria this may be im-
proved to about 40% fers another approach
2
biopsy.
(4 months)
cancer,
with
in the
no
In 67 women,
a specific
gical biopsies for benign It is of additional value
the lesion is small or in a fatty breast).
for planning
lumpectomy by obviating biopsy.
conditions. to the sur-
Our
therapy
or mastectomy), preoperative
results
indicate
sound results
(eg,
In only
one
is
or deeply In the
case
specific
agnosis
sion spite
sonographic (eg, when situated case of
X-FNA may be not but therapeutic.
correct
X-FNA
di-
It may be argued 37 lesions could with ultra-
(20,21). However, may be equivocal
cysts, nostic
diagcan
theresurgical
that
benign
agnosis was rendered by means of XFNA and cytology. Fifty-five percent (37 of 67) of these benign lesions proved to be cysts. that many of these have been diagnosed
be used
of
untoward
outcome.
(1). X-FNA ofto the evalua-
when a specific cytologic of carcinoma is made that
other
diagnosis
known
tion of nonpalpable mammographic abnormalities. To be useful, X-FNA should enable further separation of benign from malignant lesions, thereby reducing the number of sum-
geon nosis
The
woman had a small (1-cm diameter) carcinoma and negative lymph nodes and was treated with lumpectomy and irradiation. Both patients have done well. Hence, only one patient to whom mammographic follow-up was recommended had a significant
DISCUSSION cult
1
dined
as a
density.
Group
was
only there
benign
actually cytologic
an
in-
cytologic
(fibmoadenoma)
was the
diag-
di-
when
the
a carcinoma. results, this
a useful test but not without limitations. Fifty-five percent of the lesions in our series for which surgical biop-
patient (follow-up
sy was
A major problem with X-FNA is how to interpret those aspirates that provide insufficient cellular material or cellular samples containing only a few normal mammary epithelial
performed
proved
to be carci-
noma. This mate of cancer detection at surgical biopsy is about two-to-three times greater than that in many other reported series. Stated differently, if surgical biopsy was done in all 181 lesions (215 minus 34 lesions without adequate would
have
follow-up), been
the 41/181,
cancer rate or 23%, a
rate similar to that in most studies. Hence, 107 (181 minus 74) women were possibly spared surgical biopsy by the use of X-FNA. The question then arises, are we delaying cancer diagnosis by the use of X-FNA? Two
of nine
women
with
mammogmaphic
low-up
studies
to have
One
after
carcinomas
of these
progressive
changes
women
on
X-FNA at surgical
initially
their
fol-
proved
requested surgical mammography
le-
De-
biopsy had been
suggested).
cells, blood, and/or adipose tissue. our study, 116 lesions yielded this type of aspirate (group 1). From a practical
management
consider
these
for diagnosis
position,
samples
(note
contain adequate a cytology report)
decisions
we
inadequate
that
they
numbers and base
solely
In
may of cells clinical
for
on mammographic
and clinical 41 cancers
findings. We had 12 of (29%) in cytology group 1;
immediate suspicious
surgical biopsy mammograms
biopsy.
on
de-
unique
all
but
one.
This
to X-FNA.
is not
In the
based on was done a problem
Azavedo March
et 1990
al study
(16),
1 1 1 of 429
proved cancers (26%) stereotactic guidance “normal”
cytologic
The
large
tology
several varying pemience
of lesions
1 is probably
in cy-
due
reasons. Radiologists technique, expertise, performed aspirations
this study. It may be crease group 1 reports
possible with
ing
may
experience.
planation
This
for
the
fewer
errors
due
ment
is important,
small masses (12,18). Recent
to
with and in
be one
misplace-
especially
used
for
a stereotactic
de-
vice for breast aspirations, demonstrated excellent localization and mesults, even with small lesions. Stereo-
tactic methods localizations specific
should produce better and a decrease in non-
cytologic
of aspirated pending
on
the
mass.
that pies
46% were
results.
material the
The
would
cellular
Hann
amount
vary
de-
makeup
of
et al demonstrated
of their “inadequate” samhypocellular at histology
appearing
density). Table
as a mammographic
pirated.
the
results
and seen
difference
obtained
when
microcalcifications
Eighty-two
cers
and
are as-
percent
as mammogmaphic
or densities sults (groups
had positive 3, 4), but
cancers
demonstrating
cations
gave
4-month
mammography mammography
followed 8 months
a subsequent
follow-up
(ie, a 12-month fact that a physician
X-FNA mapid me-
of
A simi-
a simple
cyst.
for suspicious diagnosis
ultimately
require
the
surgeon,
logist, cessful
U
masses to detect Since our results
these with
tions
have
poorer
with
noncalcifying
ties,
we
Volume
been currently
174
biopsies with cal-
than
use
Number
#{149}
X-FNA
3
1.
2.
with
19 cancers. micmocalcifica-
masses
3.
those
and
densiless
16.
when We
a
are
and patient X-FNA.
cytologic
is essential
fre-
4.
18.
find-
when benign findings
cooperation
17.
of
19.
among cytopatho-
for suc-
References
ment is probably involved. Surgical biopsy was recommended to all 19 patients whose cancer manifested as
or calcifications
15.
X-
integration
Close
carcinomas demonstrating only, such as comedo Additionally, sampling to incorrect needle place-
14.
currently using and comparing stemeotacticaily guided FNA with XFNA. However, treatment decisions
mammographer,
more
Since
lesions
is desired.
are pmesent.
yielding
13.
FNA can be performed quickly and since cytologic results are immediately available, we occasionally perform
calcified
only
follow-up is is not a valid
ment of low-suspicion nodules or densities when sonography does not
and
cifications
9.
10.
X-FNA is an imperfect but clinically useful procedure. In about half of cases, a specific benign or malignant aspirate resulted in a clinical decision to follow up or administer definitive treatment. We currently use X-FNA primarily as an adjunct in manage-
especially cytologic
Thirty-nine in patients
results and 26
12.
that further This clearly
ings (10,16), but nonspecific
calcifications. were performed
at
cycle). Despoke
do not think mandatory.
mammographic
cells than calcifications carcinomas. error due
8.
11.
lar trend was noted by Lofgren et al (10), although this did not appear to be a problem for Hann et al (15). This difference may be due to solid noncarcinomas
7.
mammogra-
of 104 patients (25%) did not return. Notwithstanding advice to the contrary, some patients and even occasionally some physicians may believe that a “negative” cytologic result is tantamount to a negative biopsy and
masses cytologic only 56%
results.
up
to all these patients about the of mammography and cytology the follow-up recommendations,
of can-
micmocalcifi-
positive
with
For pa-
we recommend
unilateral by bilateral
demonstrate 4 highlights
in cytologic
masses
phically,
6.
to all
is compliance
followed
5.
assumption.
(15). Additionally, it must be remembered that a cytology report of mammary epithelial cells, blood, and/or adipose tissue may truly represent the type of tissue being sampled (eg, asymmetric but normal glandular tissue
being
later
common
recommendations.
24 months spite the
and microcalcifications work by Dowlatshahi
et al (1 1), who
problem endeavors
tients
by Loffor sam-
preferring
follow-up or definiWe still occasionally per-
Another follow-up
ex-
calcifications,
form X-FNA for suspicious calcifications, since a positive aspirate may permit a one-stage (with frozen-section confirmation) surgical approach. clinical
nonspecific
to needle
for
mammographic tive biopsy.
ex-
to deincreas-
cytologic results in the study gren et al (10). The potential pling
quently
results.
number
group
histologically
aspirated with had “sparse” or
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#{149}