diagnostic-therapeutic management of atypical breast lesions · galactocele and fat tissue lesions...

Review Article

Rev. Argent. Radiol. 2018;82(3): 114-123114

AbstractBreast lesions are divided histologically into two large groups: malignant and benign. Malignant lesions may be of ductal or lobular origin, with infiltrating ductal carcinoma being the most frequent invasive neoplasm. Benign breast lesions are classified as non-proliferative, proliferative without atypia and proliferative with atypia. The last two classifications include entities with a high risk of developing breast carcinoma, such as atypical ductal hyperplasia, radial scar or lobular neoplasia. We reviewed the nature of these entities and their main imaging features, primarily on mammography and ultrasound scans. When one of these diagnoses is histologically made by biopsy, it is important to review the imaging features and the type of procedure performed (number of cylinders obtained, needle gauge ...) for an appropriate subsequent management. In some cases, management will consist in complete surgical resection of the lesion, while in others, percutaneous excision (through vacuum needle biopsy) or even close imaging follow-up may be performed. Through different cases, we will share our experience and we will make a review of the current literature to recall these entities and reach adequate consensus on their management.Keywords: atypical duct hyperplasia, radial scar, lobular neoplasia, phyllodes tumor, breast lymphoma

IntroductionBenign breast lesions are classified into three groups accord-ing to their histopathological characteristics.1-5

1. Non-proliferative lesions. These entities are not associ-ated with a higher risk of breast carcinoma.1 This group would include simple cysts, epithelial-related calcifications, galactocele and fat tissue lesions such as lipomas and fat necrosis.

2. Proliferative lesions without atypia. These entities are associated with a slight, approximately 1.5- to 2-fold in-crease in the risk of developing carcinoma as compared with the general population.2-5 This group would include entities such as usual ductal hyperplasia, intraductal papil-loma, sclerosing adenosis and radial scar. Fibroadenomas would also belong to this classification6, but only if they show a complex histologic structure, are associated with adjacent proliferative disease or the patient has a family history of breast cancer.

3. Proliferative lesions with atypia. This group includes le-sions such as atypical ductal hyperplasia, lobular neoplasia (a collective term for atypical lobular hyperplasia and lobu-lar carcinoma in situ) and flat epithelial atypia. The risk of

carcinoma is three- to five-fold increased as compared with the general population, and this diagnosis may even be indicated by the presence of concomitant malignancy.7

4. Miscellaneous. Among atypical breast lesions there is a fourth group that includes entities such as breast lym-phoma or other benign lesions such as granular cell tumor, inflammatory lesions and mesenchymal tumors.

Nowadays, at the imaging diagnosis departments, it is very common to perform biopsies of breast lesions that are visible on mammography, ultrasound or even magnetic resonance imaging. Often, imaging tests are performed as screening tests in asymptomatic patients, while in other cases, these tests are ordered for symptoms such as discomfort, a nodule detected on palpation, discharge from the nipple, etc.Automated or semi-automated core-needle biopsies (CNB) may be performed using a needle ranging in size from 11 to 16 gauge, which allows different sizes of specimens to be ob-tained. The needle is inserted several times through a single opening in the skin of the patient, obtaining an average of four to five cylinders per biopsy.When vacuum-assisted biopsy (VAB) is performed, in addition to cutting tissue, the system performs an aspiration of the lesion, obtaining larger cylinders with a more representative

Diagnostic-therapeutic Management of Atypical Breast LesionsM. Delgado Márquez1 J. Rodríguez Arango2

1 Imaging Diagnosis Department, Hospital Universitario 12 de Octubre, Madrid, Spain.2 Imaging Diagnosis Department, Hospital MD Anderson Cancer Center, Madrid, Spain


M. Delgado Márquez et al.

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specimen (from nine to eleven gauge). In general, through a single cut in the skin, several samples may be drawn and ac-cumulate in a collection chamber at the back of the needle. The mean number of cylinders obtained is eight to twelve, with this type of biopsy being especially reserved for the as-sessment of microcalcifications. When the result obtained from a breast biopsy is atypical lesion, it is very important to consider the type of biopsy procedure used, the number of cylinders obtained and the type of lesion biopsied (nodule, calcification, distortion, etc.). We should also ensure that the sample has been adequately processed at the pathology de-partment.As the needle can only withdraw a limited amount of tissue and the imaging finding may be underestimated, when ob-taining one of such results, it is important to correlate imag-ing and histologic findings to decide on the future approach, preferably in consensus with a multidisciplinary committee.

In this article, we will review some of the most common atypi-cal lesions by means of examples, as well as their most appro-priate management according to a review of the literature.

Papillary Lesions

Papillary lesions of the breast (Fig. 1) are arborescent prolifer-ations of the ductal epithelium, with a fibrovascular pedicle. These lesions develop in the lumen, attached to the walls at any point in the ductal system, from the nipple to the most peripheral terminal duct-lobular unit. These lesions account for less than 3% of solid breast lesions and may be solitary or multiple. According to their histologic classification, they may be divided into benign, atypical and malignant, with the latter including intraductal carcinoma and invasive papillary carcinoma.

Fig. 1 Florid papillomatosis. Fifty-two year-old woman who presented with induration in the left breast. (A) Digital mammogra-phy. Focal asymmetry with higher density on the upper outer quadrant (UOQ) of the left breast (arrowheads). (B) Ultrasound. Hypoechoic nodule of irregular morphology (arrow). (C) Magnetic resonance imaging (MRI) with intravenous contrast. Contrast enhancement on the UOQ of the left breast, no mass, of regional distribution (circle). The histologic diagnosis following core-needle biopsy (CNB) was multiple papillomas. Surgical resection was performed, with final result of florid papillomatosis with atypical ductal hyperplasia.


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According to various studies, approximately 15% of lesions diagnosed as benign papilloma by core-needle biopsy (CNB) are found to be atypical or malignant after surgical excision and subsequent pathology review, with this risk being higher if the patient has multiple papillomatosis.8

Therefore, in this situation adequate management consists in complete surgical resection of the lesion, although an in-creasing number of studies favor performing a VAB in pre-viously biopsied lesions, for resection purposes. When the result of CNB is atypical or malignant papilloma, the lesion should be removed by surgery. 8-12

Radial scar

The radial scar is also known as complex sclerosing lesion when it is larger than 10 mm. It is an entity of unknown etiol-ogy, most common in women aged forty to seventy years old. This lesion is usually an incidental, non-palpable finding dis-covered on routine examination, most often when perform-ing a screening mammography.Both radiologically and histologically, this is a spiculated le-

sion (Fig. 2). It has a fibroelastotic core, while the spicules contain entrapped ducts, normally with hyperplasia and/or apocrine metaplasia. It may be associated with atypia or car-cinoma. On histologic examination of the complete lesion, approximately 10% show associated carcinoma, and it re-mains uncertain whether it is a premalignant lesion.13

The risk of developing breast carcinoma is approximately twice that of the general population (in either breast). There-fore, if when performing a biopsy, pathology results show radial scar, adequate management consists in complete surgi-cal resection.

Flat Epithelial Atypia

This entity is included within the spectrum of columnar lesions, which are intraductal alterations with cell proliferation. When the histological report indicates columnar cell hyperplasia (Fig. 3) no further treatment is required. When flat epithelial atypia is reported (Fig. 4), this refers to columnar hyperplasia with cells with mild atypia. It would be classified within the group of DIN 1 A lesions (ductal intraepithelial neoplasia).

Fig. 2 Radial scar. Asymptomatic forty-eight year-old wom-an. Digital mammography. In the inner quadrants of the left breast, a spiculated lesion with parenchymal distortion (ar-row) was identified, with these criteria being suspicious of malignancy. CNB with subsequent surgical resection was per-formed, and radial scar was diagnosed.

Fig. 3 Columnar hyperplasia. Sixty-two year-old asymptomatic woman. Magnified digital mammography. Cluster of coarse heterogeneous microcalcifications (arrows) of new onset as compared with previous studies. Vacuum-assisted biopsy (VAB) was performed under stereotactic guidance, showing microcalcifications associated with benign breast tissue with columnar change and columnar hyperplasia.



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The most common findings on imaging are microcalcifica-tions, predominantly of an amorphous nature. This lesion may coexist with or be a precursor of intraductal carcinoma. In the studies performed, the percentage of underestimation is approximately 20%, that is to say, in one out of five pa-tients undergoing complete surgical resection of the lesion, we will find breast carcinoma.14 The consensus on the management of this lesion should be complete surgical resection, mainly if there is ultrasound rep-resentation. If no residual microcalcifications are left after the VAB, close imaging follow-up could be a management option.

Atypical ductal hyperplasia

Atypical ductal hyperplasia is the most common high-risk le-sion. It consists in a proliferation of atypical cells occupying a portion of the duct. This lesion is histologically similar to low-grade intraductal carcinoma, and its diagnosis as one or the other entity will depend on the number of ducts in-volved and on the extent of area involvement.15-18 This lesion increases four to five times the risk of developing invasive carcinoma for both breasts, with such risk being increased six times in premenopausal women.15 It remains unclear if, be-cause of the risk, follow-up by magnetic resonance imaging (MRI) should be an indication in these patients, although no sufficient data are currently available to recommend it. Drug therapy has also been considered for risk reduction by means

Fig. 4 Flat epithelial atypia. Fifty-one year-old asymptomatic woman. Magnified digital mammography. Cluster of amor-phous microcalcifications (arrows), which increased in num-ber as compared with previous studies. VAB was performed under stereotactic guidance, showing flat epithelial atypia. Surgical biopsy was subsequently performed after placement of a harpoon, with the result being flat epithelial atypia and multiple intraductal papillomatosis.

Fig. 5 Atypical ductal hyperplasia and intraductal carcinoma. Seventy-two year-old asymptomatic woman. Digital mammogra-phy (A) amorphous, and thin and lineal microcalcifications (circled in yellow). (B) MRI after intravenous contrast administration. Focal enhancement in a paving pattern, consistent with the microcalcifications described, with these criteria being suspicious of malignancy (arrow). VAB under stereotactic guidance showed atypical ductal hyperplasia. On complete resection of micro-calcifications, the final result was high-grade intraductal carcinoma.



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of estrogen receptor modulators (tamoxifen / raloxifene) and/or aromatase inhibitors.18

Radiologically, the most common presentation is a cluster of heterogeneous microcalcifications (Fig. 5), although it may also occur as a single nodule. The probability of a higher grade lesion on excision is approximately 87% if a CNB has been performed with 14 gauge and 15-30% if VAB has been performed with 9 gauge, even when the lesion visible on imaging (mammography or ultrasound) has been fully re-sected.16,17

Based on the above, the appropriate management of this type of lesion is surgical excision.

Lobular neoplasia

Lobular neoplasia is a collective term for atypical lobular hy-perplasia (ALH) and lobular carcinoma in situ (LCIS), with the main difference being the presence or absence of dilated acini, a finding that occurs in LCIS. These entities usually have

Fig. 6 Lobular neoplasia in situ. Forty-eight year-old woman who presented with a palpable mass on her right breast. (A) Digi-tal mammography of the right breast. Increased density of nodular morphology in the upper quadrants (delimited by yellow arrowheads). (B) Ultrasound. Hypoechoic nodule of irregular morphology and poorly-defined margins (arrow). (C) MRI with intravenous contrast. Asymmetric enhancement, no mass, with focal distribution (arrow). An ultrasound-guided CNB was per-formed, showing lobular neoplasia in situ. The same result was obtained on complete surgical resection of the lesion.



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multifocal and bilateral distribution.Rather than obligatory precursors of breast carcinoma, these lesions are risk markers for the development of invasive car-cinoma in either breast (more likely in the ipsilateral breast). Atypical lobular hyperplasia increases the risk for the develop-ment of infiltrating carcinoma by fourfold or fivefold, while lobular carcinoma in situ (Fig. 6) increases such risk by eight-fold to tenfold. 19

The imaging findings for these lesions may be calcifications or nodules. It is not uncommon that they may be associated with a different entity and identified as an incidental finding. Given their high risk for developing infiltrating carcinoma, as in the case of atypical ductal hyperplasia, MRI follow-up and medical treatment with estrogen receptors modulators and/or aromatase inhibitors have been considered for risk reduction.Adequate management of this entity consists in surgical resec-tion of the lesion if there is consistency between imaging and pathologic findings, especially in the case of lobular carcinoma in situ seen on images as a nodule. Following surgery, the rate of malignancy is 20%. There is a variant of LCIS, the pleomor-

phic type, with a more aggressive biological course and con-sidered to be a precursor of intraductal carcinoma. In this case, complete surgical resection of the lesion is always indicated.

Phyllodes Tumor

Phyllodes tumor is a fibroepithelial tumor that originates out-side the ducts and lobules, in the connective tissue. It ac-counts for less than 0.5% of breast tumors. These tumors are classified into benign (58%), potentially malignant or borderline (12%) and malignant (30%). Their most usual presentation is a solid, palpable nodule of rapid growth (Fig. 7). On ultrasound, their morphology is rounded or lobulated. These tumors usually have a heterogeneous echostructure, although they are predominantly hypoechoic. They have well-defined margins and good sound transmission.In 20% of cases, these patients have a coexisting fibroadeno-ma, and 12.5% have a personal history of fibroadenoma.20 Adequate management consists in local surgical resection

Fig. 7 Phyllodes tumor. Forty-five year-old woman with a history of fibroadenoma on the right breast who presented with a new-onset palpable nodule on the left breast. (A) Digital mammography. Bilateral nodules, the largest being located in the upper outer quadrant (UOQ) of the left breast (yellow arrow). (B) On ultrasound, it appears as a solid nodule of lobulated margins and heterogeneous echogenicity (arrow), with areas of good sound transmission. (c) MRI with IV contrast. Hypervascular nodule of well-defined margins (arrow). Both CNB and complete surgical resection histopathology reports indicated Phyllodes Tumor.



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with a 1-2 cm margin as they are prone to local recurrence. In cases of large tumors, mastectomy should be performed. Ax-illary lymph node dissection is not necessary, as axillary lymph node spread is rare.

Nodular Fasciitis

Nodular fasciitis is a benign proliferative lesion of fibroblasts and myofibroblasts, most frequently located in the soft tis-sues of the arm, head and neck. When located in the breast, which is very rare, its presentation is similar to that of a car-cinoma (Fig. 8). It usually occurs as a single, hard nodule of rapid growth and irregular morphology.21

Adequate management consists in complete removal of the lesion with no further treatment, as it has a low rate of recur-

rence, with spontaneous resolution of the lesion having been occasionally reported.

Granular Cell Tumor

Granular cell tumor is a rare lesion, of uncertain histogen-esis, that appears to originate from Schwann cells. This tumor may develop in any part of the body and at any age, being most common in the head and neck region, particularly in the tongue.22 When located in the breast, it is usually found in the upper inner quadrant (UIQ), along the supraclavicular nerve which innervates the breast skin. This would be one criterion for differentiating the granular cell tumor from car-cinoma, which is most commonly located in the upper outer quadrant (UOQ).

Fig. 8 Nodular Fasciitis. Fifty-two year-old woman who reported a new-onset palpable nodule. (A) Digital mammography. Nodule in the UOQ of the right breast (arrow). (B) On ultrasound, hypoechoic nodule of rounded morphology and poorly-defined margins. (C) MRI with intravenous contrast. Solid nodule with ring-like enhancement and a hypointense center (arrow). Ultrasound-guided CNB was performed, showing a spindle-cell mass with mild atypia. On complete surgical resection of the nodule, a final diagnosis of nodular fasciitis was made.



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This tumor usually appears as a firm, non-tender mass that may cause skin retraction and nipple inversion, and a final di-agnosis cannot be established without a biopsy (Fig. 9). Most of these tumors are benign, with approximately 2% being malignant.Adequate management consists in local excision, and recur-rence is not rare. Breast Lymphoma

Breast lymphoma accounts for 0.5% of all breast cancers, with the B-cell, non-Hodgkin lymphoma being the most common subtype. There are two different entities, undistin-guishable on imaging and histologic examination: one is the primary breast lymphoma and the other is a secondary lym-phomatous involvement, which is more common.Approximately 1 to 2% of all lymphomas occur in the breast,

being most frequent in postmenopausal women. There may be unilateral or bilateral involvement. This lesion may oc-cur as: a) a solitary mass; b) multiple masses;23,24 c) infiltra-tive pattern (Fig. 10), less common, consisting in general-ized increased density of the breast parenchyma and fat on mammography. When a diffuse infiltrative pattern is found, differential diagnosis should be made among various enti-ties: breast lymphoma, inflammatory carcinoma, mastitis or venous congestion (due to heart failure or compromised ve-nous return).

Anaplastic Large-Cell Lymphoma

Anaplastic large-cell lymphoma is a very rare entity. Approxi-mately 200 cases have been reported in the literature, with 6 of them being bilateral. It is a breast implant-associated T cell lymphoma (CD30-, ALK-). The most common presentation is

Fig. 9 Granular cell tumor. Thirty-year-old male who reported a new-onset lump in the lower quadrants of the left breast. (A) Digital mammography. A surface nodule was observed, with skin thickening in the lower quadrants of the left breast (arrow). (B) Ultrasound. Hypoechoic oval nodule (arrow). (C-D) MRI (T1-weighted sequence with no intravenous contrast administration and post-contrast administration) showed that the nodule has poorly-defined margins and early contrast enhancement (ar-rows). Biopsy and surgical resection histopathology reports indicated granular cell tumor.



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a late (> 1 year) periprosthetic seroma of unexplained origin that cannot be attributed to other causes such as trauma or infection (Fig. 11).The etiology of this entity is unknown, apparently resulting from an exaggerated immune response. Diagnosis requires ultrasound-guided fine-needle aspiration biopsy (FNAB) and cytological examination of the periprosthetic fluid.25 Once di-agnosis has been made, adequate management consists in implant removal and complete capsulectomy. In most cases, no chemotherapy or radiotherapy is needed.Therefore, in the presence of periprosthetic seroma of unex-plained origin, it is recommended that FNAB be performed to rule out this entity.

Conclusions

With the implementation of breast screening programs and the large number of biopsies being currently performed at the radiology departments, histologic diagnosis of a prolifera-tive lesion, with or without atypia, has become increasingly frequent.Management of atypical breast lesions is a controversial is-sue, as many of these lesions are associated with malignancy

at high rates, while others are a risk marker for the develop-ment of carcinoma. For this reason, it is important to assess the imaging features and the type of procedure performed (number of cylinders obtained, needle gauge…) for an ap-propriate subsequent management.In some cases, management will consist in complete surgical resection of the lesion, while in others, percutaneous exci-sion (through vacuum needle biopsy) or even close imaging follow-up may be performed.

Conflicts of interestThe authors declare no conflicts of interest.

Ethical responsibilities Protection of human subjects and animals. The authors de-clare that no experiments were performed on humans or ani-mals for this investigation.

Confidentiality of data. The authors declare that they have followed the protocols of their work center on the publication of patient data.Right to privacy and informed consent. The authors declare that no patient data appear in this article.

Fig. 10 Breast lymphoma. Seventy-year-old patient who presented with induration in the periareolar region of the right breast. (A) Digital mammography. Slightly asymmetric increase in density, of nodular morphology in the retroareolar region of the right breast. (B) Ultrasound. Skin thickening with hyperechogenicity of the subcutaneous fat and small layers of fluid (arrow and circle). Biopsy report indicated infiltration due to low-grade B lymphoproliferative process.



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