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© 2008 by the American Institute of Ultrasound in Medicine
J Ultrasound Med 27:75-82 • 0278-4297

Sonographic Differentiation of Benign and Malignant Papillary Lesions of the Breast

Tae Hee Kim, MD, Doo Kyoung Kang, MD, Sun Yong Kim, MD, Eun Ju Lee, MD, Yong Sik Jung, MD and Hyunee Yim, MD

Departments of Diagnostic Radiology (T.H.K., D.K.K., S.Y.K., E.J.L.), General Surgery (Y.S.J.), and Pathology (H.Y.), Ajou University, School of Medicine, Suwon, Korea.

Address correspondence to Doo Kyoung Kang, MD, Department of Diagnostic Radiology, Ajou University Medical Center, San 5, Woncheon-Dong, Yongtong-Gu, Suwon, Kyongi-Do 442-749, Korea. E-mail: kdklsm{at}ajou.ac.kr


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective. The purpose of this study was to evaluate sonographic findings of breast papillary lesions and the effectiveness of the American College Radiology Breast Imaging Reporting and Data System sonographic assessment system for differentiation of benign and malignant papillary lesions. Methods. We retrospectively reviewed breast sonographic findings of 46 surgically proven benign papillomas and 22 papillary carcinomas. All sonographic images of patients were interpreted by 2 radiologists. Sonographic findings were analyzed according to the Breast Imaging Reporting and Data System classification. Results. The shape of the lesion was round or oval in 33 benign lesions (71.7%) and 13 papillary carcinomas (61.9%). As for the margin, a circumscribed margin was found in 31 benign papillomas (67.4%) and 12 malignant lesions (57.1%). Differences in the predominant shape and margin between the 2 groups were not statistically significant (P > .05). Fourteen benign papillomas (30.5%) and 12 papillary carcinomas (57.1%) showed a complex echo pattern. It was more frequently observed in malignant lesions; however, it was not statistically significant (P = .09). A nonparallel orientation, an echogenic halo, posterior acoustic enhancement, and associated microcalcification were more frequently found in malignant than in benign lesions (P < .05). When the presence of any suspicious sonographic feature (nonparallel orientation, echogenic halo, posterior enhancement, or calcification) was considered to indicate malignancy, interpretation of the sonographic features gave sensitivity of 85.7%, specificity of 64.9%, a positive predictive value of 47.4%, and a negative predictive value of 92.5% for detection of malignant papillary lesions. The only differential finding between noninvasive and invasive papillary cancers was a circumscribed margin (P < .05). Conclusions. Sonographic features more specific to malignancy include a nonparallel orientation, an echogenic halo, posterior acoustic enhancement, and associated microcalcification.

Key Words: breast • papillary neoplasm • sonography

Abbreviations: BI-RADS, Breast Imaging Reporting and Data System • FNA, fine-needle aspiration


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
A papillary lesion of the breast is identified histologically by the presence of a fibrovascular core and includes a spectrum of variable disease entities. These include benign intraductal papilloma, atypical papilloma, ductal carcinoma in situ with a papillary growth pattern, and invasive papillary carcinoma. There is considerable overlap in the pathologic findings between benign and malignant papillary lesions, and it can be difficult to cytologically differentiate benign papilloma from papillary carcinoma. Abruption of the myoepithelial cell layer is an important feature suggesting malignancy.1

To our knowledge, few reports about the sonographic findings of papillary lesions of the breast exist, and there has been no definitively recognized differential findings between benign and malignant papillary lesions. Furthermore, most cases were reviewed before application of the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS)2 to sonography. Therefore, the purpose of this study was to evaluate the sonographic findings of breast papillary lesions and the effectiveness of BI-RADS sonographic assessment for differentiation of benign and malignant papillary lesions.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
We retrospectively reviewed the breast sonographic findings of 46 surgically proven benign papillary tumors in 44 patients in our hospital from March 1, 2003, through January 31, 2007. We also reviewed the sonographic features of 22 malignant lesions in 17 patients from January 1, 2000, through January 31, 2007. Of 44 patients with benign papillomas, 2 patients had 2 lesions in the same breast. Of 17 patients with malignant lesions, 4 patients had multiple lesions: 2 lesions in 3 patients and 3 lesions in 1 patient.

Of 22 malignant lesions, 13 lesions were noninvasive papillary carcinomas, and 9 lesions were invasive papillary carcinomas (Table 1Go). The mean age of the patients with benign lesions was 42.1 years (range, 26–49 years), and that of those with malignant lesions was 53.7 years (31–57 years).


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  		Table 1. Results of 68 Pathologic Examinations of Breast Papillary Lesions
 
Of the 61 patients, 12 had nipple discharge, which was bloody in 5. Forty-seven patients had a palpable mass.

Sonographic Examinations
All sonographic examinations were performed by the same radiologists (D.K.K. and T.H.K) who interpreted the sonographic images. Each patient was evaluated with real-time sonography using an Acuson Sequoia 512 system (Siemens Medical Solutions USA, Inc, Mountain View, CA) with an 8- to 13-MHz linear array transducer.

Sonographic findings were analyzed according to the BI-RADS sonographic classification. The presence of a mass, shape of the mass, orientation of the lesion, margin, lesion boundary, echo pattern, posterior acoustic features, surrounding tissue changes, and presence of calcification were recorded.

Histopathologic Evaluations
Of 46 benign papillary lesions, fine-needle aspiration (FNA) was performed in 23 lesions, and core needle biopsy was performed in 3 lesions. Both FNA and core needle biopsy were done in 1 lesion. Nineteen benign lesions showed relatively typical clinical and sonographic findings, and direct surgical excision without preoperative biopsy was performed. Five lesions that showed nondiagnostic or fibrocystic changes on FNA also had surgical excision without additional biopsy.

Of 22 papillary carcinomas, FNA was performed in 17 lesions, and core needle biopsy was performed in 1. Both FNA and core needle biopsy were performed in 3 lesions. One case of papillary carcinoma showed relatively typical sonographic findings suggesting malignancy, and direct surgery without biopsy was performed. A modified radical mastectomy was performed in 13 lesions, and a partial mastectomy was performed in 9.

In the Department of Pathology, the surgical specimens were serially sliced at 5-mm intervals, prepared as paraffin-embedded sections, and stained with hematoxylin-eosin. The sections stained in each case were reviewed by 1 experienced pathologist (H.Y.) without knowledge of the breast sonographic findings.

The histopathologic results of FNA and core needle biopsy are summarized in Table 2Go. There was no case of histologic underestimation on core needle biopsy.


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  		Table 2. Histologic Results of FNA and Core Needle Biopsy
 
Statistical Analysis
The SPSS version 11.0 statistical package for Windows (SPSS Inc, Chicago, IL) was used for statistical analysis. The {chi}2 and Fisher exact tests were used, and P < .05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The sonographic appearances of benign and malignant papillary lesions are summarized in Table 3Go.


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  		Table 3. Sonographic Features of Benign and Malignant Papillary Lesions
 
One papillary carcinoma showed only a dilated duct in the subareolar area without a definite mass on sonography and was excluded from statistical analysis. The histologic finding for this lesion on surgical excision was intraductal papillary carcinoma with focal microinvasion.

The shape of the lesion was round or oval in 33 benign lesions (71.7%) and 13 papillary carcinomas (61.9%). As for the margin, a circumscribed margin was found in 31 benign papillomas (67.4%) and 12 malignant lesions (57.1%). Differences in the predominant shape and margin between the 2 groups were not statistically significant (P > .05).

Twenty-five benign papillomas (54.3%) and 6 papillary carcinomas (28.6%) were isoechoic. Fourteen benign papillomas (30.5%) and 12 papillary carcinomas (57.1%) showed a complex echo pattern. This pattern was more frequently observed in malignant lesions; however, it was not statistically significant (P = .09).

A nonparallel orientation, an echogenic halo, posterior acoustic enhancement, and associated microcalcification were more frequently found in papillary carcinomas than in benign lesions (P < .05; Figure 1Go). When the presence of any suspicious sonographic feature (nonparallel orientation, echogenic halo, posterior enhancement, or calcification) was considered to indicate malignancy, interpretation of sonographic features gave sensitivity of 85.7%, specificity of 64.9%, a positive predictive value of 47.4%, and a negative predictive value of 92.5% for detection of malignant papillary lesions.


Figure 1
Figure 1
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  		Figure 1. Invasive papillary carcinoma in a 35-year-old woman. A, Transverse sonogram shows an oval shape, a circumscribed margin, and a hypoechoic mass in the lower outer quadrant of the left breast. There is posterior acoustic enhancement. B, Color Doppler sonogram shows increased vascularity of the mass.

 
Of the benign papillomas, 21 lesions showed a solid nodule of less than 1 cm within a single dilated duct in the subareolar area. Intraductal solid nodules showed a well-circumscribed margin and a round or oval shape in 12 cases (Figure 2Go) and an indistinct margin and an irregular shape along the dilated duct in 9 cases (Figure 3Go). A cyst with an intracystic solid mass was found in 7 benign papillomas, and this lesion was described as round or oval with a circumscribed margin and a complex echoic pattern (Figure 4Go). The remaining 18 benign lesions showed a single solid mass in an extraductal location without adjacent duct dilatation (Figures 5Go and 6Go).


Figure 2
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  		Figure 2. Transverse sonogram from a 49-year-old woman with an intraductal papilloma shows a 0.4-cm round isoechoic mass within a dilated duct in the subareolar area of the right breast. There is associated microcalcification.

 

Figure 3
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  		Figure 3. Radial sonogram from a 68-year-old woman with an intraductal papilloma shows a dilated duct and an internal solid mass in the subareolar area of the left breast. This mass shows an irregular shape, a poorly defined margin, and an isoechoic pattern.

 

Figure 4
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  		Figure 4. Transverse sonogram from a 47-year-old woman with an intraductal papilloma shows a complex echoic mass in the upper inner quadrant of the right breast. This mass shows an oval shape and a well-circumscribed margin. There is posterior acoustic enhancement.

 

Figure 5
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  		Figure 5. Transverse sonogram from a 71-year-old woman with a benign papilloma shows a complex echoic mass in the upper inner quadrant of the left breast. This lesion shows an irregular shape and an angular margin, mimicking a malignant lesion.

 

Figure 6
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  		Figure 6. Transverse sonogram from a 38-year-old woman with a benign intraductal papilloma shows a single dilated duct and an isoechoic mass in the subareolar area of the right breast. This mass shows an extraductal location, an oval shape, and a circumscribed margin. There is no posterior acoustic change.

 
With regard to tumor invasiveness, the sonographic features of noninvasive and invasive papillary carcinomas are summarized in Table 4Go. Noninvasive papillary carcinomas more frequently showed a circumscribed margin than invasive papillary carcinomas (P = .03; Figure 7Go). Differences in the shape, orientation, echo pattern, lesion boundary, posterior acoustic features, calcification, and duct dilatation were not statistically significant (P > .05).


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  		Table 4. Sonographic Features of Noninvasive and Invasive Papillary Carcinomas
 

Figure 7
Figure 7
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  		Figure 7. Intracystic papillary carcinoma in a 64-year-old woman. A, Transverse sonogram shows an oval shape, a circumscribed margin, and a complex echoic mass in the upper inner quadrant of the right breast. There is posterior acoustic enhancement. B, Color Doppler sonogram shows increased vascularity in the septum and the solid portion of the mass.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Papillary lesions of the breast account for less than 10% of benign breast lesions, and invasive papillary carcinomas represent only 2% of all breast cancers.1 Because of the rarity of breast papillary lesions, especially malignant lesions, there have been few reports about the sonographic findings, and most of them were reviewed before application of the BI-RADS to sonography.

Intraductal papillomas and papillary carcinomas have considerable overlap in imaging features,3 and it is more difficult to differentiate them on sonography than other breast neoplasms. This is because malignant papillary lesions frequently show a round or oval shape and a circumscribed margin, which are suggestive findings of benign lesions in other breast neoplasms.

In our study, of 46 benign papillomas, 21 lesions showed the well-known "typical" finding of intraductal papillomas, which was a solid nodule within a single dilated duct in the subareolar area. There is little difficulty in diagnosing these typical benign intraductal papillomas. However, benign papillomas showing a single mass in an extraductal location without adjacent duct dilatation may mimic malignant lesions, especially if the lesions show an irregular shape, a noncircumscribed margin, or a complex echo pattern.

Han et al4 classified benign papillary lesions into 4 types according to the relationship between the mass and the duct: type I, intraluminal mass; type II, extraductal mass; type III, purely solid mass; and type IV, mixed. In their study, 26 (65%) of 40 benign papillary lesions showed a circumscribed margin sonographically. In our study, a circumscribed margin was found in 31 (67.4%) of 46 benign papillomas, showing results similar to those of Han et al.4 However, 12 (57.1%) of 21 papillary carcinomas also showed a circumscribed margin in our study, suggesting that it could not be the differential finding for benign and malignant papillary lesions.

Lee et al5 classified breast papillary lesions as a cystic or ductal type or a solid type, and the shape, wall change, margin, internal echo pattern, posterior echo changes, and other associated findings for the 2 types were analyzed. They concluded that in cystic or ductal lesions, a poorly defined irregular thick cystic wall, a poorly defined irregular margin, heterogeneous mixed internal echoes, and posterior enhancement suggested malignancy, and in solid lesions, posterior enhancement was more frequently found in malignant than in benign lesions. They thought that posterior enhancement was more frequently seen in papillary carcinomas because of mucin production, which cannot be seen in benign papillomas. Our results also showed that posterior acoustic enhancement was a characteristic finding of papillary carcinomas (P < .05).

Lam et al6 reported sonographic findings of breast papillary lesions according to the BI-RADS classification. They considered any of the following as suspicious for malignancy: an irregular mass, any lesion not parallel to the skin line, any noncircumscribed margin, a complex echo pattern, posterior acoustic shadowing or a combined pattern, Cooper ligament changes, skin thickening, edema, architectural distortion, and skin retraction or irregularity. They also reported that of all 16 malignant lesions, 9 showed 1 or more sonographically suspicious features, and the remaining 7 appeared benign on sonography; the sensitivity of sonography for detection of malignant papillary lesions was 56%. In our study, an irregular shape, a noncircumscribed margin, and a complex echo pattern were more frequently seen in papillary carcinomas, but they were not statistically significant.

In contrast to the result of Lam et al,6 posterior acoustic enhancement was a characteristic finding of malignant papillary lesions in our study. This result is similar to that of Lee et al.5 They reported that solid papillary carcinomas were frequently associated with mucin production, which was not found in benign papillomas, and that might be why posterior enhancement was a characteristic finding of papillary carcinomas.5

There is controversy over treatment of papillary neoplasms. Some have reported that papillary lesions diagnosed as benign on core needle biopsy should be surgically excised because of a histologic upgrade at excision and a relatively low negative predictive value (83%).6,7 Others have concluded that when the histologic diagnosis on core needle biopsy is benign and concordant with imaging findings, the lesions could be safely managed with follow-up imaging rather than with surgical excision.8–10 In our study, of 22 papillary carcinomas, FNA was performed in 17 lesions, and core needle biopsy was performed in 1. Both FNA and core needle biopsy were performed in 3 lesions. There were 12 cases of histologic underestimation on FNA but no case on core needle biopsy.

In our study, a nonparallel orientation, an echogenic halo, posterior enhancement, and associated calcification were characteristic findings of papillary carcinomas, and when the presence of 1 or more of these findings was considered to indicate malignancy, the sonographic features gave sensitivity of 85.7%, specificity of 64.9%, a positive predictive value of 47.4%, and a negative predictive value of 92.5%. Our results showed a relatively high negative predictive value and no case of histologic underestimation on core needle biopsy. Therefore, we expect that when the histologic diagnosis on core needle biopsy is benign and concordant with the sonographic findings, these lesions can be safely managed with follow-up imaging.

There were several limitations in our study. First, the data group was small, and further investigation with a larger data set is needed. Second, our study was a retrospective interpretation of the sonographic findings of breast papillary lesions. Therefore, the vascularity of the lesions was not evaluated in all examinations. Papillary lesions of the breast are highly vascular tumors and have a propensity to bleed spontaneously.3 Han et al4 reported that spontaneous intracystic bleeding is more suggestive of malignant papillary lesions. If the vascularity of the lesions had been evaluated in all cases of our study, increased vascularity or an increased blood supply pattern could have been a differential finding for malignant lesions and benign papillomas. Third, in our study, there was no case of histologic underestimation on core needle biopsy. However, core needle biopsy was done in only 4 benign and 4 malignant lesions. Therefore, a further larger study is needed to conclude that when the histologic diagnosis on core needle biopsy is benign and concordant with the sonographic findings, follow-up imaging is enough.

Although the sonographic features of breast papillary carcinomas may overlap with those of benign papillomas, features more specific to malignancy include a nonparallel orientation, an echogenic halo, posterior acoustic enhancement, and associated microcalcification. Although it is not always possible to differentiate papillary carcinomas from benign papillomas on the basis of sonography, familiarity with these features will aid in suggesting the correct diagnosis and treatment plan.


   Footnotes
 
Received June 11, 2007, from the Departments of Diagnostic Radiology (T.H.K., D.K.K., S.Y.K., E.J.L.), General Surgery (Y.S.J.), and Pathology (H.Y.), Ajou University, School of Medicine, Suwon, Korea. Revision requested July 11, 2007. Revised manuscript accepted for publication August 29, 2007.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Tavassoli FA. Papillary lesions. In: Tavassoli FA (ed). Pathology of the Breast. Norwalk, CT: Appleton & Lange; 1992:193–227.
  2. American College of Radiology. ACR Breast Imaging Reporting and Data System Breast Imaging Atlas. Reston, VA: American College of Radiology; 2003.
  3. Ganesan S, Karthik G, Joshi M, Damodaran V. Ultrasound spectrum in intraductal papillary neoplasms of breast. Br J Radiol 2006; 79:843–849.[Abstract/Free Full Text]
  4. Han BK, Choe YH, Ko YH, Yang JH, Nam SJ. Benign papillary lesions of the breast: sonographic-pathologic correlation. J Ultrasound Med 1999; 18:217–223.[Abstract]
  5. Lee CS, Kook SH, Shin HJ, et al. Papillary tumors of the breast: US findings of benign and malignant lesions. J Korean Radiol Soc 2000; 42:871–876.
  6. Lam WW, Chu WC, Tang AP, Tse G, Ma TK. Role of radiologic features in the management of papillary lesions of the breast. AJR Am J Roentgenol 2006; 186:1322–1327.[Abstract/Free Full Text]
  7. Mercado CL, Hamele-Bena D, Oken SM, Singer CI, Cangiarella J. Papillary lesions of the breast at percutaneous core-needle biopsy. Radiology 2006; 238:801–808.[Abstract/Free Full Text]
  8. Rosen EL, Bentley RC, Baker JA, Soo MS. Imaging-guided core needle biopsy of papillary lesions of the breast. AJR Am J Roentgenol 2002; 179:1185–1192.[Abstract/Free Full Text]
  9. Liberman L, Bracero M, Vuolo MA, et al. Percutaneous large core biopsy of papillary breast lesions. AJR Am J Roentgenol 1999; 172:331–337.[Abstract/Free Full Text]
  10. Sydnor MK, Wilson JD, Hijaz TA, Massey HD, Shaw de Paredes ES. Underestimation of the presence of breast carcinoma in papillary lesions initially diagnosed at core-needle biopsy. Radiology 2007; 242:58–62.[Medline]




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