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ORIGINAL ARTICLE
Year : 2019  |  Volume : 15  |  Issue : 4  |  Page : 864-870

Breast hamartoma: Ultrasound, elastosonographic, and contrast-enhanced ultrasound features


1 Department of Radiology, Chinese People's Liberation Army General Hospital, Beijing, China
2 Department of Ultrasound, Chinese People's Liberation Army General Hospital, Beijing, China

Date of Web Publication14-Aug-2019

Correspondence Address:
Zhi Li Wang
Department of Ultrasound, Chinese People's Liberation Army General Hospital, 28 Fuxing Road, Beijing 100853
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_711_18

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 > Abstract 


Aims: To present the ultrasound (US), shear-wave elastography (SWE), and contrast-enhanced ultrasonography (CEUS) features of breast hamartomas.
Subjects and Methods: In this retrospective analysis, we included 36 breast hamartomas of 36 female patients who had been scheduled for US-guided vacuum-assisted biopsy (VAB) or surgical excision between May 2013 and October 2016. In the 36 patients, US, CEUS, and SWE were performed, and the pathology results from surgical or VAB were obtained. The US, SWE, and CEUS features of the lesions were analyzed.
Results: All breast hamartomas had an oval-shaped and a circumscribed margin. Of the 36 hamartomas, 30 (83.3%) had heterogeneous echogenicity and 28 (77.8%) displayed no changes in posterior echogenicity. There were no significant differences in the maximum, mean, and minimum elasticity between the hamartomas and peripheral parenchyma (P = 0.885, 0.683, and 0.451, respectively). All hamartomas appeared with a clear edge on CEUS, and none showed lesion diameter expansion after the injection of contrast. Compared with the peripheral parenchyma, 10 hamartomas (27.8%) showed rapid perfusion mode, 23 (63.9%) showed equal perfusion mode, 24 (66.7%) showed equal enhancement, and 9 (25.0%) showed hyperenhancement. The mean peak intensity and area under the curve of hamartomas were significantly higher than those of peripheral parenchyma (P = 0.013 and P = 0.011, respectively). The peak time and increasing-start time were not significantly different between hamartomas and peripheral parenchyma (P = 0.321 and P = 0.215, respectively).
Conclusions: Hamartomas have typical features on US, SWE, and CEUS. Applying multiple ultrasound techniques would be helpful for their diagnosis.

Keywords: Breast, contrast-enhanced ultrasound, elasticity, hamartoma


How to cite this article:
Liu G, Wang ZL, Zhang MK, He Y, Liu Y. Breast hamartoma: Ultrasound, elastosonographic, and contrast-enhanced ultrasound features. J Can Res Ther 2019;15:864-70

How to cite this URL:
Liu G, Wang ZL, Zhang MK, He Y, Liu Y. Breast hamartoma: Ultrasound, elastosonographic, and contrast-enhanced ultrasound features. J Can Res Ther [serial online] 2019 [cited 2019 Nov 20];15:864-70. Available from: http://www.cancerjournal.net/text.asp?2019/15/4/864/264300




 > Introduction Top


Hamartomas are benign formations that can develop in various organs, including the kidneys, lungs, skin, and breasts.[1],[2] Breast hamartomas represent a disorganized overgrowth of mature breast elements. These lesions were initially described in 1971 by Arrigoni et al.;[3] they account for 0.1%–0.7% of all benign mammary masses and are most commonly reported among middle-aged women.[4],[5],[6] However, with the increasing awareness and widespread breast cancer screening, more and more hamartomas could be routinely diagnosed.

Breast hamartomas contain glandular epithelium, adipose tissue, and fibrous tissue in variable proportions.[7] Hamartomas appear in a wide spectrum of variation when using ultrasound (US), with a general heterogeneous internal echo pattern. The broad-range US appearances of hamartomas due to the differing ratios of tissue elements restrict the diagnostic role of US.[8] Thus, contributions of other modalities to the diagnosis of hamartomas are important.

In recent years, new techniques of US, including elastosonography and contrast-enhanced ultrasonography (CEUS), have developed rapidly. Shear-wave elastography (SWE) is a new method of obtaining elastography images. With this method, the radiation force is produced by the probe rather than the operator. In prior studies, SWE has shown potential for differentiating benign from malignant breast diseases and could possibly reduce the overall number of breast biopsies.[9],[10],[11],[12],[13] CEUS can offer detailed information on tumor vascularity.[14] Studies have demonstrated the role of CEUS in the differentiation of benign and malignant breast lesions.[15],[16] To the best of our knowledge, there have been no wide series reports of the application of SWE and CEUS in the diagnosis of breast hamartomas.

Thus, the purpose of this study was to present the SWE and CEUS features of breast hamartomas and to analyze the diagnostic performance of these techniques in the differentiation of benign and malignant breast lesions.


 > Subjects and Methods Top


Patients

A total of 1216 breast lesions in 1165 consecutive women who had been scheduled for US-guided vacuum-assisted biopsy (VAB) or surgical excision between May 2013 and October 2016 were initially included in this study. Of those, 36 lesions in 36 patients were diagnosed as breast hamartoma. The US, SWE, and CEUS features of these lesions were analyzed. The study was approved by our local ethics committee. Written informed consent was obtained from every patient at enrollment.

The age range of the 36 patients was 23–65 years (mean age ± standard deviation, 42.1 ± 22.3 years). The largest diameter of all the lesions was 1.1–6.5 cm (mean diameter ± standard deviation, 3.38 ± 2.15 cm). Thirty-two of the 36 women (88.9%) presented with symptoms including palpable breast lesion (30, 83.3%) and breast pain (5, 13.9%).

Histological diagnoses were obtained for all lesions via US-guided 7G VAB (10, 27.8%), or surgical excision (26, 72.2%). All diagnoses were made by a pathologist with 20 years of experience in breast pathology, who was blinded to the US results.

US examinations

US examinations were performed using the iU22 ultrasound system (Philips Medical Systems, Andover, Massachusetts, USA) with a L12-5 linear array probe. The examinations were performed by two experienced breast radiologists who have 12 years and 11 years of experience in breast US, respectively. The radiologists were unaware of any clinical information or of the histopathological diagnosis at the time of the US examination. The time of examination was 10–16 min (mean time ± standard deviation, 18.6 ± 5.1 cm).

The patients were lying in supine or lateral position. The location, largest diameter, border, echogenicity, and the coexistence of calcifications in the breast lesions were examined by US. Color Doppler was used to detect the blood signal within and surrounding the breast lesions. Alder's semi-quantitative method was used to classify the blood signal as follows: level 0, no blood signal within the lesion; level I: a poor blood flow, with 1–2 patchy blood signals; level II: moderate blood signals, with a main blood vessel whose length was longer than half of the lesion, or several small blood vessels; and level III, rich blood signals, with more than four blood vessels or netted blood vessels.

Shear-wave elastography

Aixplorer ® ultrasound system (SuperSonic Imagine, Aix en Provence, France) with a 15-4 MHz linear array probe was used for elastosonography. The probe was applied as light as possible in order to avoid pressure to the lesion. The probe needs to be kept still for 10–20 s during acquisition of the elastography images (due to a slow frame rate), and this was often best done during a breath hold. The elastography views that were selected were those that were most clearly displaying abnormal stiffness within the plane in the absence of movement or pressure artifact, such as the red area under the probe. After a stable image was obtained, the image was recorded, and the region of interest (ROI) was chosen to calculate the elasticity value. The size and location of ROI was standardized as follows: the ROI was chosen to be as large as possible, to cover the whole lesion. Attempts were made such that the ROI in the peripheral parenchyma is of the same size and depth as the ROI in the corresponding breast lesion. The maximum value within the ROI, called max elasticity, the mean elasticity, and the minimum value within the ROI, called min elasticity, were recorded. For each patient, three ROIs were selected in the lesion and peripheral parenchyma, and the mean value was regarded as the final value.

Two radiologists who performed the SWE imaging measured the quantitative SWE features.

Contrast-enhanced ultrasound

The iU22 ultrasound system (Philips Medical Systems, Andover, Massachusetts, USA) was used, with L9-3 broadband linear array probe, as well as the conditions of pulse reversed phase harmonic contrasting. The mechanical index was 0.07. The ultrasound contrast agent was Sonovue (Bracco Milan, Italy), which was oscillation-diluted with 5 ml of saline before use. During the examination, 5 ml of contrast agent was intravenously bolus-injected through the medial cubital vein, and 3-min continuous dynamic US images were synchronously and dynamically stored in the instrument.

Offline analysis of the stored image data was performed, and the features of the enhanced contrasting lesion areas were then carefully observed, including 5 indicators: contrast perfusion mode (rapid, equal, or slow perfusion), enhanced homogeneity of lesion areas (homogeneous, heterogeneous), whether or not the lesion diameter expanded when the contrast agent reached the peak (expansion, nonexpansion), whether or not the edge was clear (clear, not clear), and lesion intensity at the peak (low or iso enhanced and highly enhanced). The above indicators were used as the qualitative diagnostic basis of lesions. The QLAB analysis software was also used. The ROI were selected to be in the most enhanced portions of the lesions in macroscopical ultrasonography images. Attempts were made that the ROI in the peripheral parenchyma is of the same size and depth as that of the corresponding hamartoma nodule. For each patient, three ROIs were selected in the tumor and peripheral parenchyma, respectively, and the mean value was regarded as the final value. Subsequently, time-intensity curve was performed and the perfusion parameters could be obtained through the curve, including the peak intensity, area under the curve, peak time, and increasing-start time.

Two radiologists, who performed the CEUS, measured the quantitative CEUS parameters.

Statistical analysis

All analyses were performed using SPSS 17.0, standard version (SPSS Inc., Chicago, IL, USA). The Student's t-test was used for the comparison of quantitative parameters of both elastography and CEUS. Comparison between groups was done using the Chi-square test.

Variabilities in reader final assessment categories were calculated with κ statistics. A κ value of 0.20 or less was considered slight; 0.21–0.40, fair; 0.41–0.60, moderate; 0.61–0.80, substantial; and 0.81–1.00, almost perfect. P < 0.05 was considered statistically significant.


 > Results Top


US features

[Table 1] shows the US features of breast hamartomas. All breast hamartomas had an oval shape and a circumscribed margin. Of the 36 breast hamartomas, 30 had heterogeneous echogenicity (83.3%, 30/36) and 28 were without changed posterior echogenicity (77.8%, 28/36). None of the breast hamartomas showed level III blood.
Table 1: Ultrasound features of breast hamartomas (n=36)

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Elastosonographic features

The max, mean, and min elasticity of breast hamartomas are presented in [Table 2]. There was no significant difference in the max elasticity (P = 0.885), mean elasticity (P = 0.683), and minimum elasticity (P = 0.451) between hamartomas and peripheral parenchyma [Figure 1].
Table 2: Elasticity parameters of breast hamartomas

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Figure 1: Shear-wave elastography image of a hamartoma in the right breast of a 39-year-old female. (a) Heterogeneous lesion on conventional ultrasound; (b) Shear-wave elastography image showed the max and mean elasticities of hamartoma, which were similar to the normal tissue

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Although the max elasticity and mean elasticity of the hyperechoic area were slightly higher than those of the hypoechoic area, there were no statistically significant differences in the max elasticity and mean elasticity between the hyperechoic and hypoechoic areas within the hamartomas [Figure 2] and [Table 3].
Figure 2: Shear-wave elastography image of a hamartoma in the right breast of a 42-year-old female. (a) Heterogeneous lesion on conventional ultrasound; (b) Shear-wave elastography image showed the max and mean elasticities of hyperechoic area within the hamartoma, which were slightly higher than those of the hypoechoic area, but without statistical significance

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Table 3: Elasticity parameters of different parts of breast hamartomas

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Contrast-enhanced ultrasonography features

The contrast perfusion mode, enhanced homogeneity, lesion diameter expansion, edge, and peak intensity of hamartomas are presented in [Table 4]. All hamartomas appeared with a clear edge. None of the hamartomas showed lesion diameter expansion after the injection of contrast. Compared with the peripheral parenchyma, 10 of the 36 hamartomas (27.8%) showed rapid perfusion mode, 23 (63.9%) showed equal perfusion mode, 24 (66.7%) showed equal enhancement, and 9 (25.0%) showed higher enhancement [Figure 3] and [Figure 4].
Table 4: Contrast-enhanced ultrasonography features of breast hamartomas (n=36)

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Figure 3: Contrast-enhanced ultrasonography image of a hamartoma in the left breast of a 38-year-old female. (a) Heterogeneous lesion on conventional ultrasound; (b) Contrast-enhanced ultrasonography image showed the enhancement pattern of hamartoma which was similar to that of the peripheral parenchyma, and the edge of the lesion was very clear

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Figure 4: Contrast-enhanced ultrasonography image of a hamartoma in the left breast of a 35-year-old female. (a) Heterogeneous lesion on conventional ultrasound; (b) Contrast-enhanced ultrasonography image showed the enhancement pattern of hamartoma which was higher than that of the peripheral parenchyma, and the edge of the lesion was very clear

Click here to view


The mean peak intensity and area under the curve of the hamartomas were significantly higher than those of the peripheral parenchyma (P = 0.013 and P = 0.011, respectively). There were no significant differences in the peak time and increasing-start time between the hamartomas and the peripheral parenchyma (P = 0.321 and P = 0.215, respectively) [Table 5].
Table 5: Quantitative contrast-enhanced ultrasonography parameters of breast hamartomas

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Reproducibility

Reliability of the quantitative elasticity measurements on the SWE images was good for the max, mean, and min elasticity values. The max, mean, and min elasticities were all reliable measurements, with intraclass correlation coefficient (ICC) = 0.87, 0.81, and 0.79, respectively.

Reliability of the quantitative CEUS measurements was good for the peak intensity, area under the curve, peak time, and increasing-start time. Peak intensity, area under the curve, peak time, and increasing-start time were all reliable measurements, with ICC = 0.87, 0.82, 0.88, and 0.79, respectively.


 > Discussion Top


Breast hamartomas have also been referred to as lipofibroadenomas, adenolipofibromas, and fibroadenolipomas. The US presentations of hamartomas differ widely owing to the marked variability in the fatty and fibrous tissue contents. It has been reported that, on US, most mammary hamartomas have circumscribed margins, an oval shape, and heterogeneous internal echogenicity.[17] Studies have reported that the heterogeneous echogenicity of hamartomas, with hypoechoic areas intermixed with hyperechoic band-like or nodular areas, reflects the presence of fatty, epithelial, and fibrous connective tissues. The hypoechoic area often represents the fatty and epithelial components, whereas the hyperechoic area often represents the fibrous components. Studies have reported that hamartomas in which fatty or epithelial tissue occupies the major part often appear as homogeneous hypoechoic, whereas hamartomas in which fibrous tissue occupies the major part often appear as homogeneous hyperechoic.[18]

The result of this study is similar to that of the previous studies in that all hamartomas appeared as oval shape with a circumscribed margin. Thirty cases (83.3%) in this study appeared as heterogeneous echogenicity and 28 cases (77.8%) appeared without changed posterior echogenicity. Only four hamartomas (11.1%) appeared as hypoechoic lesions and two hamartomas (5.6%) appeared as hyperechoic lesions. This meant that most hamartomas had fatty, epithelial, and fibrous tissues inside, which resulted in the heterogeneous echogenicity.

In this study, hypervascularization was absent on color Doppler imaging. No lesions demonstrated level III blood flow, and only three cases (3.8%) demonstrated level II blood flow. This result is similar to that of the previous studies,[19] which demonstrates that hamartomas are benign breast lesions that are not rich in blood flow, which might be helpful for the differentiation with the other breast lesions that are rich in blood flow, such as intraductal papilloma.

Different tissues of the breast have distinct elastographic features, with fibrous and glandular tissues displaying greater stiffness than the fat tissue.[20],[21] The elastosonographic appearance of hamartoma depends on the amount of fibrous tissue. In previous studies, hamartoma was less elastic than the peripheral parenchyma.[22] However, in this study, there was no significant difference in the max, mean, and min elasticity between the hamartomas and peripheral parenchyma. The difference might be caused by the different way of choosing ROI. Because the ROI box was a circle and it was hard to cover the whole lesion, we made the best efforts to cover the most part of the lesion. The tissues in the ROI were diverse, such as glandular epithelium, adipose tissue, and fibrous tissue, and the mixed tissue decreased the max and mean elasticities of the ROI area.

A previous study demonstrated that the elasticity of the hyperechoic area was significantly higher than that of the hypoechoic area.[22] However, in our study, interestingly, although the max elasticity and mean elasticity of the hyperechoic areas were slightly higher than those of the hypoechoic areas within the hamartomas, there were no statistically significant differences. This discrepancy in the findings of the studies might be related to the different way of choosing ROI, which should be further studied.

In this study, hamartomas had specific characteristics on CEUS. All hamartomas appeared with a clear edge. None of the hamartomas showed lesion-diameter expansion after the injection of contrast. Most hamartomas showed rapid (27.8%) or equal (63.9%) perfusion mode and equal (66.7%) or higher (25.0%) enhancement compared with the peripheral parenchyma. The specific appearance of hamartomas was helpful for the differential diagnosis with the other breast lesions.

This study showed that the mean peak intensity and area under the curve of hamartomas are significantly higher than those of the peripheral parenchyma. However, this sign could also be seen in other kinds of benign breast lesions, such as fibroadenomas.[23] Thus, in the diagnosis of hamartomas by CEUS, other kind of parameters should be considered as well, such as the enhancement mode, lesion-diameter expansion, edge, and peak intensity. Furthermore, the US characteristics and elastographic characteristics should also be considered in the diagnosis of hamartomas by CEUS.

Malignant transformation of hamartomas is a very rare event, but it can occur because the mass contains epithelial tissue. There have been reports about malignant neoplasia (both lobular and ductal carcinoma inclusive) arising within hamartomas.[24],[25],[26],[27] However, there is no way of confirming this as being derived from the hamartoma itself or as an incidental finding. In this study, there were no findings of malignant transformation from the hamartomas.

There are some limitations to this study. First, mammography was not included in this study. Some patients were directly referred for a VAB or surgery because of the large volume of the lesion. Some studies have reported that hamartomas are typically seen on mammography as oval or round formations, and are easy to be diagnosed if they have typical performance.[28] Further study could be done for the comparison of US and mammography in the diagnosis of hamartomas. Second, we did not include the malignant lesions and the other benign lesions in this study. Further study could compare the difference between hamartomas and other lesions in US, elastography, and CEUS appearance.


 > Conclusions Top


Hamartomas have typical features on ultrasound, elastography, and CEUS. Applying multiple US techniques would be helpful for the diagnosis of hamartomas.

Acknowledgment

Financial supports from the National Natural Science Foundation (81771832) and capital characteristics of the fund (Z161100000516190) are gratefully acknowledged.

Financial support and sponsorship

Financial supports for this study were received from the National Natural Science Foundation (81771832) and capital characteristics of the fund (Z161100000516190).

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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