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Sonographically Depicted Breast Clustered Microcysts: Is Follow-Up Appropriate?

¹ Johns Hopkins Greenspring, 10755 Falls Rd., Suite 440, Lutherville, MD 21093.

Received June 11, 2004; accepted after revision November 15, 2004.

 
Correspondence to W. A. Berg (wendieberg{at}hotmail.com).

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. The objective of this study was to evaluate outcomes of lesions prospectively classified on breast sonography as clustered microcysts without a discrete solid component.

SUBJECTS AND METHODS. Over a 4-year interval during which 1,900 consecutive breast sonography examinations were obtained at the University of Maryland, 110 examinations (5.8%) yielded 123 lesions so classified. Sonography was performed by a physician using a linear-array broadband transducer (L7.5–12 or L7–13 MHz). Follow-up of at least 24 months was available for 66 lesions, and 14-gauge core biopsy was performed on another 13 lesions. The median patient age was 48 years (range, 32–71 years), and the median lesion size was 8 mm (range, 5–30 mm).

RESULTS. Of the 79 lesions with acceptable follow-up, all were depicted sonographically, 57 (72%) were seen mammographically, and four (5%) were palpable. Of the 13 lesions biopsied, five (38%) showed apocrine metaplasia; five (38%), fibrocystic changes; two (15%), cysts; and one (8%), a microscopic fibroadenoma and cysts. Of the 66 lesions with 2-year follow-up, 35 (53%) were stable, 15 (23%) had resolved, 12 (18%) decreased, and four (6%) minimally increased at 1 year and were then stable (n = 2) or decreased (n = 2) after 2 subsequent years. Fusion of several small cystic spaces was seen in one (2%) of the lesions followed.

CONCLUSION. Breast clustered microcysts are relatively common, seen in 5.8% of breast sonograms. In our series of 79 lesions with follow-up, none proved malignant: Follow-up on an annual basis appears reasonable for most such lesions. Validation of this approach across multiple centers is needed.

Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
A variety of types of cystic lesions of the breast have been described [1]. Most simple cysts are readily characterized as anechoic, circumscribed masses with posterior enhancement and can be dismissed as benign [2]. Complex cystic lesions, with mixed cystic and solid components, a thick wall or thick septations, or an intracystic mass merit biopsy, with 23% of such lesions proving malignant in the series of Berg et al. [1]. Clustered microcysts have been defined as lesions consisting of a cluster of tiny anechoic foci that individually are 2–3 mm with thin (< 0.5 mm) intervening septations and no discrete solid component [3]. Follow-up of lesions that manifest as clustered microcysts has been proposed as an alternative to biopsy [4]. The purpose of this study was to determine the outcome of a consecutive series of breast lesions that manifest as clustered microcysts on sonography.

Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
From August 1997 through December 2001, during performance of 1,900 consecutive breast sonography examinations, I prospectively identified 110 examinations (5.8%) and 123 lesions consisting of clustered microcysts. Recording and reviewing the results of these examinations and the results of subsequent imaging, clinical, and histopathologic follow-up was approved by the institutional review board. Of the 1,900 examinations, 1,658 (87.3%) were targeted to a mammographic or clinical abnormality and that quadrant of the breast was scanned. For 242 of the examinations (12.7%), the whole breast was scanned for an indication of newly diagnosed cancer, high-risk screening in dense breasts, or presumed fibroadenoma in a woman under 30 years old.

Sonography was performed by a physician using a linear-array broadband transducer (Performa [L7.5–12 MHz], Acoustic Imaging; or Elegra [L7–13 MHz], Siemens Medical Solutions). Spatial compounding was used when available. The sonographic diameter of each lesion was recorded in three planes (radial, antiradial, and anteroposterior). Sonographic follow-up was recommended at 6, 12, and 24 months, and the results were prospectively recorded.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —52-year-old woman with clustered microcysts. Spot magnification craniocaudal mammogram shows circumscribed, microlobulated mass.

View larger version (148K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —52-year-old woman with clustered microcysts. Radial L7.5-12–MHz sonogram (Performa, Acoustic Imaging) shows clustered microcysts. This lesion resolved on follow-up mammography.

View larger version (168K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —58-year-old woman on hormone replacement therapy with incidental clustered microcysts on screening sonography (performed due to dense breast tissue). Radial (A) and antiradial (B) L7–13–MHz sonograms with spatial compounding (Elegra, Siemens Medical Solutions) show lesion composed of tiny anechoic foci ranging from 1 to 5 mm. This lesion was stable on 36 months' follow-up.

View larger version (185K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —58-year-old woman on hormone replacement therapy with incidental clustered microcysts on screening sonography (performed due to dense breast tissue). Radial (A) and antiradial (B) L7–13–MHz sonograms with spatial compounding (Elegra, Siemens Medical Solutions) show lesion composed of tiny anechoic foci ranging from 1 to 5 mm. This lesion was stable on 36 months' follow-up.

Biopsy or imaging follow-up of at least 24 months was considered acceptable follow-up. Our radiology and pathology databases were queried for follow-up for all 110 women with clustered microcysts prospectively identified. For lesions biopsied by patient or physician choice, histopathologic findings were recorded; all lesions biopsied were also followed for at least 24 months after biopsy. When biopsy was performed, sonographically guided core biopsy technique was used. Briefly, with the patient under local anesthesia, a 14-gauge Monopty gun (Bard Urological) was used under direct sonographic visualization to obtain from three to six samples. Follow-up of at least 24 months (range, 24–68 months; mean, 42 months) was available for 66 lesions (61 breasts), and 14-gauge core biopsy was performed on another 13 lesions (13 breasts). Incomplete follow-up of 6–16 months was available for another 22 lesions, with no malignancies identified; these lesions were not considered in further analyses.

View larger version (163K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3 —32-year-old woman with incidental clustered microcysts on screening sonography (performed due to high risk). Transverse L7–13–MHz sonogram with spatial compounding (Elegra, Siemens Medical Solutions) shows clustered microcysts, one of which contains low-level echoes (arrow) due to debris within the fluid—that is, a complicated microcyst. This lesion resolved at 12 months' follow-up.

View larger version (134K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A —57-year-old woman with palpable mass due to clustered microcysts that enlarged and then regressed on follow-up. Mediolateral oblique mammogram shows indistinctly marginated mass corresponding to palpable abnormality (marked with a radiopaque marker).

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B —57-year-old woman with palpable mass due to clustered microcysts that enlarged and then regressed on follow-up. Transverse L5–10–MHz sonogram (equipment details not available) obtained at another institution shows irregular hypoechoic mass considered suspicious, with biopsy initially recommended.

Top Abstract Introduction Subjects and Methods Results Discussion References

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C —57-year-old woman with palpable mass due to clustered microcysts that enlarged and then regressed on follow-up. Transverse L7.5–12–MHz sonogram (Performa, Acoustic Imaging) shows lesion to correspond to clustered microcysts. Follow-up was recommended instead of biopsy.

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D —57-year-old woman with palpable mass due to clustered microcysts that enlarged and then regressed on follow-up. Transverse L7.5–12–MHz sonogram at 5 months' follow-up shows slight enlargement in several anechoic spaces. Continued follow-up was recommended.

View larger version (83K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4E —57-year-old woman with palpable mass due to clustered microcysts that enlarged and then regressed on follow-up. Transverse L7–13–MHz sonogram with spatial compounding (Elegra, Siemens Medical Solutions) at 41 months' follow-up shows moderate decrease in overall size of lesion and regression of individual microcysts.

View larger version (164K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A —48-year-old woman with clustered microcysts shown with improved technique. Antiradial L7–13–MHz sonogram without spatial compounding (Elegra, Siemens Medical Solutions) shows irregular hypoechoic mass initially considered suspicious with biopsy recommended.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B —48-year-old woman with clustered microcysts shown with improved technique. Antiradial L7–13–MHz sonogram with spatial compounding and application of increased pressure while scanning shows lesion to be clustered microcysts. Lesion was followed and had decreased at 26 months' follow-up.

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A —75-year-old woman with invasive lobular carcinoma manifest as new indistinctly marginated mass mammographically. Radial L5–12–MHz sonogram (HDI 3500, Philips-ATL) shows hypoechoic lesion thought to possibly represent clustered microcysts.

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B —75-year-old woman with invasive lobular carcinoma manifest as new indistinctly marginated mass mammographically. Antiradial (B) and radial (C) L7–13–MHz sonograms with spatial compounding (Elegra, Siemens Medical Solutions) show hypoechoic mass with angular (arrow, C) and indistinct margins. Spatial compounding helps to better depict angular and indistinct margins, which facilitates classification of this as suspicious mass needing biopsy. Sonographically guided 14-gauge core biopsy showed invasive lobular carcinoma.

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6C —75-year-old woman with invasive lobular carcinoma manifest as new indistinctly marginated mass mammographically. Antiradial (B) and radial (C) L7–13–MHz sonograms with spatial compounding (Elegra, Siemens Medical Solutions) show hypoechoic mass with angular (arrow, C) and indistinct margins. Spatial compounding helps to better depict angular and indistinct margins, which facilitates classification of this as suspicious mass needing biopsy. Sonographically guided 14-gauge core biopsy showed invasive lobular carcinoma.

Of 13 lesions biopsied because of patient or referring physician preference, five (38%) revealed apocrine metaplasia; five (38%), fibrocystic changes; two (15%), cysts; and one (8%), a microscopic fibroadenoma and cysts. On follow-up after biopsy, nine (69%) of 13 resolved (including the fibroadenoma) and the other four (31%) decreased.

Of 66 lesions with at least 24 months' follow-up, 35 (53%) were stable, 15 (23%) were gone, and 12 (18%) decreased. Another four (6%) increased initially by 2–5 mm in maximal diameter without any other concerning change. In two of these enlarging lesions, individual microcysts enlarged or possibly fused to form larger cystic spaces (Figs. 4A, 4B, 4C, 4D, and 4E). These four initially enlarging lesions continued to be followed and were stable (n = 2) or decreased (n = 2) (Figs. 4A, 4B, 4C, 4D, and 4E) over at least another 2 years' follow-up (range of total follow-up, 40–66 months).

Technique was noted to be critical to proper interpretation. Three of the 79 lesions had been recommended for biopsy by another radiologist. In these three lesions, a 7.5-MHz transducer was used initially. Rescanning with increased pressure and a high-frequency transducer (center frequency, 10 MHz) allowed proper identification of the lesion as clustered microcysts (Figs. 4A, 4B, 4C, 4D, 4E, 5A, and 5B), and these three lesions were followed. A fourth lesion was initially questioned as being clustered microcysts at another facility, but on repeat scanning, it was prospectively recognized as having indistinct and angular margins sonographically and mammographically and was new mammographically; it was biopsied, and the results showed invasive lobular carcinoma (Figs. 6A, 6B, and 6C).

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Breast sonography is used routinely to further characterize circumscribed and indistinctly marginated masses seen mammographically, to evaluate palpable breast masses, and to guide biopsy or aspiration of spiculated masses [5–7]. There is increasing interest in whole-breast sonography both to evaluate the extent of disease [8–10] and to supplement screening for women with dense breasts [11–16]. A practical deterrent to the widespread use of any screening test, including screening breast sonography, is the finding of incidental indeterminate lesions that require biopsy yet prove benign. Across multiple single-center studies of screening breast sonography [11–16], on average, 2.8% of the women screened underwent biopsy, with 11.4% of the biopsied lesions proving malignant [17]. Another 2.8–10.3% of patients were recommended for short-interval follow-up in those series [11–16].

For a breast lesion to be dismissed as benign, BI-RADS category 2 [18], or to be classified as probably benign, BI-RADS category 3 [18], certain criteria have to be met. Benign lesions should have no greater risk of malignancy than the surrounding parenchyma. Probably benign lesions should have a low rate of malignancy, and follow-up of those few lesions that prove malignant should not adversely affect prognosis [19]. For mammography, particular lesions have been described that have less than 2% risk of malignancy, including circumscribed, nonpalpable masses of any size [20–24] and clustered punctate calcifications on a baseline mammogram [20, 25].

The criteria for classifying breast lesions seen only on sonography as probably benign are less well established [26]. Stavros et al. [27] proposed criteria for differentiating benign from malignant solid nonpalpable masses on sonography and have been able to maintain a rate of malignancy of less than 1% among masses classified as benign in their practice. Widespread validation of this approach is still needed. The classification of lesions as probably benign has to date been restricted to nonpalpable lesions, although further study of this issue is warranted. Rahbar et al. [28] applied the criteria of Stavros et al. in reviewer studies and found a 4% rate of malignancy among lesions classified as probably benign. In retrospect, none of the misclassified cancers met the criteria for a benign lesion, and three of the four misclassified cancers were palpable [28]. In a series of lesions going to biopsy, Hong et al. [29] reported 16/372 (9%) of sonographically oval, circumscribed masses proved malignant, though they comment that those lesions were likely either enlarging, palpable, or had mammographically suspicious features. In a recent series, Graf et al. [30] reported no malignancies among 157 palpable circumscribed noncalcified masses that appeared benign on both mammography and sonography.

In this series, no malignancies among the 79 lesions prospectively classified as clustered microcysts, including four palpable lesions, were found. I now routinely follow such lesions in 1 year, if they are well seen, or in 6 months if the features are not optimally depicted (e.g., deep or small lesions < 5 mm). If there is any question of a solid component, I recommend biopsy using core technique and sonographic guidance. Complicated cysts have been described as circumscribed masses with posterior enhancement and homogeneous low-level echoes or a fluid–fluid level [31]. Nonpalpable complicated cysts can be considered probably benign, with one 3-mm ductal carcinoma in situ found among 567 lesions classified as complicated cysts across three series [32–34] (1.8% malignancy rate). Clustered microcysts can have fluid–debris levels or thick hypoechoic fluid containing debris within individual microcysts (Fig. 3). The latter, a "complicated microcyst," may be difficult to distinguish from a small solid component, and core biopsy or aspiration is reasonable in this setting if there is uncertainty.

For follow-up to be a reasonable alternative to biopsy, patients must be compliant with such a recommendation. According to the current BI-RADS guidance [3, 18], lesions classified as probably benign were followed at 6, 12, and 24 months and then classified as benign, category 2 after 24 months' stability. I found that women whose lesions were seen mammographically were more likely to have adequate follow-up than those seen only sonographically, perhaps due to the relative lack of formalization of breast sonographic follow-up compared with the routine practice of annual mammographic surveillance and associated tracking of follow-up recommendations in our practice. In this series, adequate follow-up was achieved for 79 (64%) of 123 lesions and incomplete follow-up for another 22 (18%) of 123 lesions. This is comparable to compliance with follow-up in other breast imaging series [30, 35–39].

Careful attention to sonographic technique with the use of high-frequency transducers with center frequency of at least 10 MHz is critical for the accurate characterization of breast masses. Spatial compounding, which integrates information from off-angle beams, decreases "speckle" artifact and facilitates margin characterization, but reduces perception of posterior enhancement or shadowing [40–42]. Spatial compounding was helpful in evaluating clustered microcysts in this series (Figs. 4A, 4B, 4C, 4D, 4E, 5A, 5B, 6A, 6B, and 6C), and application of the proper amount of pressure while scanning (Figs. 5A and 5B) and the use of high-frequency transducers (Figs. 4A, 4B, 4C, 4D, and 4E) were also important. For deep lesions, harmonic imaging, in which a multiple of (usually twice) the fundamental frequency is analyzed, may also help distinguish tiny cysts from solid masses while preserving posterior features [41, 43], although further study of this issue is warranted.

Clustered microcysts represent the lobular portion of the terminal duct lobular unit, with dilatation of individual acini [4, 44]. The epithelium lining the acini can be of the usual type, as in fibrocystic changes, or undergo apocrine metaplasia and be composed of a tall secretory columnar epithelium. In this series, microcysts were equally likely to have bland epithelium as to have apocrine metaplastic epithelium. Clustered microcysts with apocrine metaplasia can show enhancement on MRI; enhancing clustered microcysts on MRI may also be followed though further study is warranted.

Apocrine metaplasia commonly is manifest as clustered microcysts, with 10 (77%) of the 13 sonographically visible lesions of apocrine metaplasia having this appearance in the series of Warner et al. [4]. In the series of Kushwaha et al. [45], eight (73%) of 11 cases of apocrine metaplasia going to stereotactic biopsy were manifest as calcifications that most often were heterogeneous and less commonly were amorphous or punctate in morphology.

It has been suggested that, over time, adjacent acini in apocrine metaplastic lobules will fuse and form larger cysts [44]. My colleagues and I observed such a change in only two (3%) of 66 clustered microcysts followed for a minimum of 2 years (Figs. 4A, 4B, 4C, 4D, and 4E).

In summary, clustered microcysts in the breast are relatively common incidental findings, seen in 5.8% of breast sonograms in this series. Clustered microcysts were most common in women 39–50 years old. In the absence of a solid component, clustered microcysts are likely benign, with no malignancies in this series. The definition of clustered microcysts as composed of 2- to 3-mm anechoic foci [3] may merit broadening to allow association with larger cystic spaces. In this series, cystic spaces within the lesion ranged from less than 1 mm up to 7 mm. Attention to proper sonographic technique, including application of sufficient pressure while scanning and use of high-frequency transducers with a center frequency of at least 10 MHz, is important in distinguishing the microcystic nature of these lesions, and spatial compounding also appears to improve characterization. When there is no discrete solid component and the lesion is well seen sonographically, based on my experience with 79 lesions prospectively classified as clustered microcysts, routine follow-up appears to be a reasonable alternative to biopsy. Further multicenter evaluation of this approach is warranted and is planned [46].

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Top Abstract Introduction Subjects and Methods Results Discussion References

 

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