Diagnostic and Interventional Imaging (2014) 95, 169—179

CONTINUING EDUCATION PROGRAM: FOCUS. . .

Complex cystic breast masses in ultrasoundexamination

A. Athanasioua,∗, E. Auberta, A. Vincent Salomonb,A. Tardivona

a Medical Imaging Department, Institut Curie, 26, rue d’Ulm, 75005 Paris, Franceb Tumor Biology Department, Institut Curie, 26, rue d’Ulm, 75005 Paris, France

KEYWORDSBreast;Breast ultrasound;Complex cysticmasses

Abstract Complex cystic masses are defined as lesions composed of anechoic (cystic) andechogenic (solid) components, unlike complicated cysts, the echogenic fluid content of whichimitates a solid lesion. Complex masses are classified as ACR4 and require histological verifi-cation by percutaneous biopsy and/or surgical ablation. The etiology is diverse, and can bebenign or high risk (an abscess, hematoma, fat necrosis, fibrocystic mastopathy, a phyllodestumor, papilloma) as much as malignant (papillary cancer, necrotic cancer, a ductal carcinomain situ, metastases). The biopsy technique must be adapted to each case and it is often neces-sary to insert a coil during the procedure. Histopathological correlation is essential to ensure

that the samples are representative and concur with the ultrasound appearance, so as not to fail to recognize high risk or malignant lesions requiring appropriate management.© 2014 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

Cysts are by far the most frequently encountered breast condition and are usually asymp-tomatic and found accidentally while performing an ultrasound examination. Cystic lesionsneed to be described and classed according to the BIRADS lexicon [1,2] (Table 1):• typically benign, simple cysts (ACR2): strictly anechoic content, imperceptible wall,

posterior acoustic enhancement;• probably benign, complicated cysts (ACR3): homogeneous hypoechoic content or with

more or less sloping fluid/fluid levels, imperceptible wall, with or without posterior

enhancement;

• complex cysts of indeterminate nature (ACR4): association of cystic and solid compo-nents, thick wall or internal septum/septa.

∗ Corresponding author.E-mail address: alexandra.athanasiou@curie.fr (A. Athanasiou).

2211-5684/$ — see front matter © 2014 Éditions françaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.http://dx.doi.org/10.1016/j.diii.2013.12.008

170

Table 1 BIRADS classification of cystic lesions.

Category Description

Simple cyst Imperceptible wallAnechoic contentPosterior acoustic enhan

Complicated cyst Thin wallEchogenic contentFluid/fluid levelPosterior acoustic enhan

Complex cystic mass Thick wall > 0.5 mmThick septa > 0.5 mmIntracystic mass

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The challenge for the radiologist is differentiatingetween a complicated cyst and a complex cystic mass.hen a solid component is revealed, even if discreet, the

esion comes into the category ACR4 (PPV between 2—95%)ith a biopsy indicated for diagnostic purposes. Indeed, the

ates of malignancy reported in the literature vary between3% and 31% depending on the paper [3—5]. The aim ofhis article is to describe how to optimize the ultrasoundechnique, the signs of complex masses, the place of theifferent techniques of percutaneous biopsy and to examinehe diagnostic range of complex masses.

xamination techniques

s for any imaging examination, it is essential to havevailable all the clinical and radiological data before per-orming and interpreting a breast ultrasound examination.he ultrasound technique (B mode) should meet the follow-

ng criteria:linear probes of frequencies between 7.5 and 20 MHz(more often 12—14 MHz) should be used. The frequencymust be adapted to the breast volume and the location ofthe lesion in the breast (lower frequency for deep lesions,high frequency for superficial lesions);total gain and TGC should be used to obtain an adequateand homogeneous signal from the skin to the depth of thepectoral muscle;the focal zone must be adjusted in depth relative to thelesion;the lesion must be analyzed in at least two planes: trans-verse and longitudinal or radial (according to the majoraxis of the lactiferous ducts) and anti-radial.

The use of additional modes helps characterize theesion; the radiologist needs to know their main characteris-ics as well as their respective advantages and disadvantagesn order to make the best use of them.

armonic mode

armonic mode improves spatial resolution and contrastf the lesion and reduces artefacts (e.g. reverberationrtefacts from cyst walls), so that posterior ultrasound mod-fications are seen better [6].

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ompound mode

ompound mode improves the signal/noise ratio by reducingackground noise and speckle artifact, optimizes analysisf the margin of the lesion and the internal echostructuref masses. It also enables better detection of intralesionalalcifications [7]. On the other hand, posterior ultrasoundodifications are attenuated [8].

oppler mode

oppler mode (color and/or power) ought to be systematic.t provides elements guiding diagnosis: perilesional hyper-mia if lesions are inflammatory (cysts, abscesses) versusntralesional vascularization indicating the solid nature ofhe lesion. In order to obtain a good Doppler map, it will beecessary to:work with PRF values of around 1000 Hz;set amplification just above the noise threshold;adjust the size of the Doppler box in order to increasesensitivity and decrease flow artifacts [9].

Power Doppler is more sensitive to slow flows but is alsoore sensitive to artifacts [10]. It should be remembered

hat the absence of a Doppler signal does not mean that theolid nature of a lesion can be excluded.

lastography

his can help characterize complicated cysts by revealinghe fluid component (trilaminar or bull’s eye appearance intatic mode, signal void appearance in shear mode). In theame way, if the lesion is found to be very hard,this will helponfirm diagnosis of complex masses and guide percutaneousiopsies (improving the histological characterization of theesion) [11,12].

ltrasound signs of complicated cysts

omplicated cysts show all the aspects of simple cystsxcept for the content, which is finely echogenic. They may

ave a fluid level or internal echoes that correspond toebris and which are displaced slowly with changes in theatient’s position. In no case do complicated cysts contain

solid parietal mass (Fig. 1).

Complex cystic breast masses in ultrasound examination 171

echoes related to the hemorrhage, and thus reveal thesolid component. If necessary, ultrasound-guided fine needleaspiration may confirm a true intracystic mass.

Ultrasound classification of complexmasses

Berg et al. have defined 4 categories of complex massesdepending on morphological criteria [4]:• cysts with a thick wall (≥ 0.5 mm);• cysts with thick internal septa (≥ 0.5 mm) (Fig. 3);• predominantly cystic complex masses (cystic components

at least 50%) (Fig. 4);• predominantly solid complex masses (at least 50% solid

components) including peripheral cystic components(Fig. 5).

Cysts with a thick wall or internalseptum > 0.5 mm

Benign conditions

• inflammatory cysts, more or less ruptured;• fibrocystic mastopathy associated with apocrine meta-

plasia. This often manifests as grouping of microcysts.

Figure 1. Complicated cyst. Well-defined round shape showing adebris/fluid level.

Assessing the mobility of the echogenic component anddetecting flow by power Doppler can be of help: if theechogenic component does not move or if no flow has beendetected, it is impossible to distinguish between a solid pari-etal mass and hemorrhagic or inflammatory debris adheringto the wall of the lesion. On the other hand, detecting aDoppler signal indicates a real parietal mass.

According to Berg et al. (ACRIN 6666 study) [4], only12% of complicated cysts reported actually seem to be solidlesions, with a malignancy rate of 0.42%. They placed theselesions in the ACR3 category and recommended follow-upat 6 months. If the size changed over 6 months by > 20%, adiagnostic biopsy was indicated [8,13].

Ultrasound signs of complex masses

The majority of complex masses show posterior acousticenhancement due to the cystic component. The margin maybe macro- or microlobulated, indistinct or even irregular.Differentiating an intracystic mass from an intraductal massis not always obvious, although intraductal masses are usu-ally tubular in appearance (Fig. 2a and b). Sometimes

intracystic hemorrhage can mask the solid component of acomplex mass. Simply moving the patient into the lateraldecubitus position may be enough to displace the internal

Figure 3. Type II complex cystic mass. This is a predominantlycystic mass, with many septa, which are > 0.5 mm thick. Cyst withhemorrhagic changes.

Figure 2. a: diagram of the development of intraductal and intracystic lesions. Initially the lesion with a solid component gradually fillsand dilates the lactiferous ducts involved. When there is considerable dilatation the lesion appears as a complex cystic mass; b: tubularintraductal lesion dilating and filling the duct (intraductal papilloma).

172 A. Athanasiou et al.

Figure 4. a: type III complex mass (intracystic mass) corresponding to a modified cyst; b: similar appearance in another patient wherepower Doppler confirmed the solid character of the parietal bud by detecting the internal vascularization. In this case, it was an intracysticpapillary carcinoma.

A simple fine needle aspiration biopsy will confirm thediagnosis;

• fat necrosis may be seen as an ultrasound mass with athick wall. There is no hyperemia in the Doppler unlessthere is secondary inflammation. A connection to the scaron the skin may confirm this diagnosis;

• collections (hematoma, seroma, lymphocele): the clinicalcontext will provide information as to whether traumaticor post-operative. (Fig. 6). Depending on the clinical pre-sentation, a first reference ultrasound examination canbe done at 4—6 months, since certain images persist forseveral months;

• a breast abscess is suggested from the clinical examina-tion when faced with the trio of fever, pain, and localhyperemia with inflammatory skin signs, occurring clas-sically in a post-partum, traumatic or surgical context.The associated risk factors are smoking, diabetes andbelonging to a black race [14]. In ultrasound, it presentsas a complex mass with posterior enhancement, and incolor Doppler, as having thick hypervascularized walls.Fine needle aspiration biopsy establishes the diagnosis

Figure 5. Type IV complex mass with a solid component ofmore than 50%, with small peripheral cystic recesses. Fibrocysticmastopathy.

and allows material to be collected for bacteriologicalanalysis (Fig. 7a—d);

• juvenile papillomatosis may be seen as a nodular imagecomposed of multiple cysts. This is not a papillary lesionbut a hyperplastic epithelial lesion which must be surgi-cally ablated (a high risk lesion) [15];

• a cystic breast lymphangioma is a rare tumor belongingto the lymphatic malformation group. It is a multiloc-ulated lesion occurring in children, female adolescentsand young women. It grows slowly. Fine needle aspira-tion biopsy will reveal the presence of lymphocytes in thefluid aspirated. Biopsy will also find the presence of lym-phoid cells thus confirming the diagnosis. There is no riskof these lesions becoming malignant, but nevertheless,because of their size, surgical ablation is indicated [16].

Malignant conditionsThese diseases are classically highly proliferative necroticcancers (poorly differentiated, grade III, necrotic invasiveductal carcinomas) (Fig. 8a and b). Nevertheless their wallsare markedly thicker and more highly vascularized. Theyare also associated with suspicious mammography signs suchas a mass with irregular, even spiculated margins, and thepresence of microcalcifications and very often axillary lym-phadenopathies (which are better explored by ultrasound).

Figure 6. Complex mass with cystic recesses and fibrin septa.Organized hematoma.

Complex cystic breast masses in ultrasound examination 173

Figure 7. a: anechoic, ovoid mass with thick posterior wall. Note the pseudo-image at the upper pole (reverberation artifact): mammaryabscess; b: mammary abscess in another patient: hypoechoic mass, containing fine echoes, thick-walled, hypervascularized with colorDoppler; c: needle aspiration cytology showed the presence, on a hemorrhagic background, of inflammatory polynuclear cells; d: favorableprogress under treatment with regression of the abscess.

Figure 8. a: breast ultrasound in a young woman to explore a palpable mass. Two contiguous lesions are visible, one hypoechoic, thick-ggest

•

•

walled with focal thickening, and with heterogeneous contents, suinvasive ductal carcinoma with marked necrosis.

Medullary cancer can also appear as a thick-walled cysticmass [17].

Predominantly cystic complex masses

Benign conditionsDifferential diagnoses include:• modified cysts with or without mobile debris (Fig. 9a—c);• post-therapeutic fat necrosis revealed as a complex ultra-

sound mass. Obviously the medical history and correlationwith the mammogram showing typical fat clarity canconfirm the diagnosis without needing a biopsy for typicalcases (Fig. 10a—c);

ing hemorrhage and/or internal necrosis; b: histology showing an

a galactocele appears as a complex mass with severalfluid/fluid levels. This image ought not to present a prob-lem of diagnosis given the context of breast-feeding.papillary lesions (benign and atypical papillomas): papil-lomas occur at 40 to 50 years of age, while the agerange for papillary cancers appearing is 63—67 years [18].Clinically, these lesions may be associated with breastdischarges, either serous (more particularly in cases ofbenign papillomas) or brownish/hemorrhagic (suggestingrather, a malignant lesion). Papillomas develop in milk

ducts which are subsequently obstructed. They usuallyappear as cystic lesions with parietal nodules (Fig. 11a).In color Doppler, intralesional flow is observed in the vas-cular stalk (Fig. 11b). These lesions should be biopsied

174 A. Athanasiou et al.

Figure 9. a: B mode ultrasonography detected an anechoic lesion with an image of focal parietal thickening; b: no signal was detectedwith color Doppler; c: shearwave elasticity image. Signal void appearance concordant with mainly fluid content. The echogenic parietal partis coded in blue; it is very soft with a value < 30 kPa An ultrasound-guided needle aspiration biopsy (14-gauge) targeted on the echogenicp

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(Fig. 11c). Histological diagnosis is based on the presenceof proliferation of ‘‘finger-in-glove’’ projections that areedged by an epithelium and have a fibrovascular core.It is difficult to tell from biopsy fragments whether apapillary lesion is benign, atypical or malignant, in situor invasive, hence the need to analyze the entire lesion[19—21]. Papillomas said to be atypical show areas ofapocrine metaplasia and/or atypical ductal hyperplasia(ADH) (Fig. 12a—c). The risk of breast cancer associated

with an atypical papilloma is similar to the risk in patientswho have ADH elsewhere in the breast (× 4—5). The risk ofbreast cancer is higher (× 7) in women with multiple atyp-ical papillomas and peripheral papillomas. Moreover, the

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igure 10. a: thick-walled complex mass including solid parietal nodass where the connection to the cutaneous scar can be clearly seen; c

ecrosis corresponding to the ultrasound image. Biopsy is not indicated

igure 11. a: complex intracystic mass; b: color Doppler examinationuggestive of a papilloma — a biopsy is indicated; c: histology after the

evertheless surgical ablation to study the whole of the lesion is recomm

risk of underestimating a papillary carcinoma is 8—14%,hence surgical ablation is recommended in order to ana-lyze the histology of the entire lesion [22].

alignant conditionsncapsulated intracystic papillary carcinomancapsulated intracystic papillary carcinoma is a rare formf cancer, representing 0.6% to 1% of breast cancers23—25]. The appearance is more heterogeneous comparedith papillomas, and often associated with hemorrhagic

hanges (Fig. 13a). Fine needle aspiration biopsy is inad-quate (Fig. 13b). A 10-G vacuum-assisted core biopsyith a post-biopsy marker is the procedure recommended.

ules: b; in another patient, the appearance of a similar complex: comparison with mammographic images found typically clear fatin this case.

detected a vascular stalk within the solid component. Appearancebiopsy showing a papilloma with no signs of atypia or malignancy.ended (risk of underestimation).

Complex cystic breast masses in ultrasound examination 175

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Figure 12. a: type III complex mass with discrete hemorrhagic cformed; c: histological results showed a sclerosing papilloma with a

Macroscopically, the mass is friable or lumpy inside a cyst(Fig. 13c). Microscopically, it consists of one or more papil-lary carcinoma nodules surrounded by a thick fibrous capsule(Fig. 13d—e).

A colloid, metaplastic or mucinous carcinomaA colloid, metaplastic or mucinous carcinoma can also looklike an intracystic mass but such an appearance is rare.

Predominantly solid complex masses

Benign conditions

• fibrocystic mastopathy;• complex fibroadenomas: these are fibroadenomas which,

as well as the dual fibrous and epithelial component, alsopresent cysts larger than 3 mm, adenosis, epithelial cal-cifications and apocrine metaplasia (Fig. 14a—b);

• phyllodes tumors with, in particular peripherally, cysticslits. Seventeen percent of phyllodes tumors are observedwith these features [26]. Surgical ablation to study theentire lesion is essential (Fig. 15a—c).

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Figure 13. a: type III complex mass; b: the first ultrasound-guided needexceptional richness of which was the reason for histological verificationof marker confirmed the presence of malignant papillary cells; c: macfriable mass inside a cyst. The post-biopsy coil is visible; d and e: microsccribriform. The axes of the papillae are bordered by multistratified carc

es; b: vacuum-assisted macrobiopsy with a 10-G system was per-ine metaplasia. Surgical ablation recommended.

alignant conditionsolid papillary carcinomaolid papillary carcinoma can either be a completely solidass (sometimes even containing microcalcifications), or aredominantly solid complex mass (Fig. 16a). Histologically,o clear papillae are observed. The underlying papillarytructure is represented by a network of fibrovascular coresmong the solid cell proliferation (Fig. 16b).

ertain ductal carcinomas in situertain ductal carcinomas in situ exhibit papillary growthharacterized by a fibrovascular core bordered by a neoplas-ic epithelium. These lesions are different from papillomaolonized by DCIS. They may be observed as complex massesontaining microcalcifications.

nvasive ductal carcinoma

nvasive ductal carcinoma, sometimes of high nuclear gradegrade III). The importance of correlation with the clini-al findings and the mammogram, as well as systematicxploration of the axilla using ultrasonography should not

le aspiration biopsy collected cells with a papillary architecture, the despite the absence of suspect cells. A macrobiopsy with insertionroscopic examination of the ablated tissue showed an indentedopic examination: essentially papillary tumor architecture, focallyinomatous cells with moderate cytonuclear atypia.

176 A. Athanasiou et al.

Figure 14. a: type IV round complex mass with essentially peripheral, cystic recesses; b: ultrasound-guided microbiopsy (14G) showing afibroadenoma.

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igure 15. a: type IV round complex mass with essentially periphumor; c: macroscopically, a solid mass was found in the ablated ti

e forgotten, to avoid misinterpreting malignant lesions.Fig. 17a and b).

nvasive lobular carcinomanvasive lobular carcinoma may also present this aspectFig. 18a—d).

are malignant lesionsther tumors also show as complex masses, such asedullary mucinous carcinoma, metaplastic carcinomas,reast sarcomas and metastases, particularly melanoma.

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igure 16. Solid papillary carcinoma. a: complex mass with a predomicrocalcifications can be distinguished; b: histological examination fobrovascular cores.

cystic recesses; b: ultrasound-guided microbiopsy (14G): phyllodesith peripheral cystic components.

nterventional diagnostic strategy

ampling techniques

omplex cystic masses are a challenge for interven-ional breast radiologists because the technical difficultys directly related to the presence of a fluid component.ndeed, aspiration of the cystic material and its collapse

uring biopsies makes the associated solid componentmperceptible or hardly perceptible and therefore moreifficult to sample with certainty. The indications for biopsyust be clear and precise, while avoiding unnecessary

inately solid component and irregular margins. Intralesional fineund a malignant papillary structure surrounded by a network of

Complex cystic breast masses in ultrasound examination 177

Figure 17. a: young woman consulting for a mass that had recently appeared in the left breast. Ultrasound exploration showed a typeIV complex mass. Given her young age fibrocystic mastopathy was wrongly suggested; b: axillary exploration on the other hand corrected

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the diagnostic error since it revealed clearly suspect axillary lymphnode invasion.

procedures. Correlation with the mammogram data and thepatient’s history is essential to avoid sampling benign com-plex masses (hematoma, fat necrosis, galactocele), wherethe alternative of close monitoring would seem to be moreappropriate.

Fine needle aspiration biopsy

For palpable complex masses, biopsy procedures should beunder ultrasound guidance to ensure correct sampling ofthe solid component. Fine needle aspiration is indicated asthe first interventional procedure when there is a problemof diagnosis between a complicated cyst and a predomi-

nantly cystic complex mass. If a purulent liquid is collected,bacteriological analysis should be requested. If the liquidis hemorrhagic, it should be sent for cytological analysis[27,28]. After any fine needle aspiration biopsy, the lesion

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Figure 18. a: type IV complex mass; b: microbiopsy performed with ainserted; d: histology indicated invasive lobular adenocarcinoma. Prolifera scleroelastotic stroma. Marked cytonuclear atypia.

s with a focally thickened cortex. It was a grade III IDC with lymph

ust be reassessed. If there is partial or complete collapsef the lesion, a post-biopsy marker should be left at the sitef the initial image [29].

iopsies

f a solid component remains after fine needle aspirationiopsy, core biopsies should be performed in the sameession; necrotic components of cancers may not containalignant cells [30].Where there is a proven solid component, core biopsies

ill be performed in the first place whenever there arenfavorable signs (microcalcifications or architectural dis-

ortion) in a mammogram. For predominantly solid lesions,

14-gauge needle is perfectly suitable. On the other hand,or lesions which are predominantly cystic and have smallarietal nodules, a vacuum-assisted macrobiopsy system

14G system; c: because of partial collapse a post-biopsy clip wasation of independent cells or cells connected in narrow lines within

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ith 8 or 10-gauge needles is preferable. If the mass is asso-iated with calcifications, an X-ray of the samples should beaken. A post-biopsy marker should always be inserted athe end of the procedure if the residual mass is difficult toee [29].

adiologic/pathologic correlation

adiologic/histopathologic concordance must be estab-ished and the lesion definitively classified (multidisciplinarytaff). It must therefore be possible to explain the signshown by each complex mass from the histopathologicalata. The pathologist must have a detailed description ofhe lesion to be able to compare the histopathological withhe ultrasound appearance.

f there is concordance

f there is concordance between the imaging and theistopathology, follow-up after 6 months can be proposedefore returning to classic monitoring, in order to minimizehe risks of false negatives [30].

ny diagnosis of lesions with a risk

ny diagnosis of lesions with a risk of underestimation (pap-llary lesion, phyllodes tumor, atypical ductal hyperplasia,n situ nodular neoplasia) requires surgical ablation; the ratef malignancy found on ablated tissue varies between 30%nd 38% [31—33]. The risk of underestimating the malig-ancy of papillary lesions is between 8% and 14% [22,34] andhis is all the greater when the papillomas are peripheralcompared with centrally located papillomas, i.e. retroare-lar).

f there is discordance

f there is discordance, the whole case should beeexamined: correct targeting, representativeness of theamples. If necessary new percutaneous biopsies or a sur-ical biopsy will be discussed.

onclusion

omplex cystic masses are lesions of an indeterminateature, classified at least as ACR4 and requiring percu-aneous biopsy and/or surgical ablation. Ultrasonographynder good conditions (correct adjustment, use of harmonicnd/or compound mode, Doppler and elastography) canharacterize these lesions and guide biopsies.

There is a wide range of diagnoses, ranging fromenign lesions (inflammatory and/or modified cyst, post-herapeutic changes, fibroadenoma) to high risk or atypicalesions (papilloma, phyllodes tumor), or even malignant

esions (intracystic papillary or solid carcinoma, necroticuctal carcinoma, lobular carcinoma). With a rate of malig-ancy varying from 23% to 31%, any complex lesion must beharacterized and carefully sampled. Papillomas and highisk lesions must be surgically ablated.

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A. Athanasiou et al.

TAKE-HOME MESSAGES• Complex masses are classified as ACR4.• They require histological verification.• Radiologic/pathologic correlation is essential

(representativeness of the samples, suitablemanagement).

• The rate of malignancy varies between 23 and 31%.

isclosure of interest

he authors declare that they have no conflicts of interestoncerning this article.

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