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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Radiographically guided fine-needle aspiration of nonpalpable breast lesions.

Radiographically guided fine-needle aspiration (X-FNA) in 215 nonpalpable, mammographically detected breast lesions was performed by means of a coordi...
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