Biomedical Imaging and Intervention Journal Follow BIIJ on Twitter Find BIIJ on Facebook

Current issue Contact us
 
 
 

Editorial Board
Instruction for Authors
Editorial Workflow
Reviewers
Events
Recorded Presentations
Remote Education

Free subscription





Subscription will allow you to receive automatic alerts and announcements from biij

13th Asian Oceanian Congress of Radiology (AOCR), Taipei, Taiwan March 20-23, 2010

5th Congress of Asian Society of Cardiovascular Imaging, Hong Kong, 18-19 June 2011

Engineering and Physical Sciences in Medicine and the Australian Biomedical Engineering Conference, Australia, 14-18 August 2011

Home > Contents

Article


Biomed Imaging Interv J 2010; 6(3):e21
doi: 10.2349/biij.6.3.e21
© 2010 Biomedical Imaging and Intervention Journal


PDF version Review Article

Mammographic and ultrasonographic features of invasive lobular carcinoma: a review of 16 patients

M Muttarak*,1MD, S Sangchan2, MD, P Kongmebhol1, MD, N Sukhamwang3, MD, B Chaiwun3, MD
1 Department of Radiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
2 Department of Radiology, Phrae Hospital, Phrae, Thailand
3 Department of Pathology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

Abstract

Objectives: To review the mammographic and ultrasonographic findings of invasive lobular carcinoma (ILC), determine the role of ultrasonography (US) in the detection of ILC, and determine if ILC is frequently missed on mammography.

Materials and methods: Approval by Institutional Review Board was granted. Between January 2000 and July 2008, medical records and pathological diagnosis of 1,146 invasive breast carcinomas at the authors� institution were retrospectively reviewed. Only patients with pathologically-proven pure ILC were included. The initial mammographic reports were analysed to determine the true-positive and false-negative rates for the detection of cancer.

Results: There were 37 patients diagnosed as pure ILC which accounted for 3% of all invasive breast carcinoma. Of the 37 patients, 16 had imaging studies and constituted the material of this study. The patients ranged in age from 45-76 years (mean age, 56.43 years). Of the 16 patients, one was asymptomatic, one presented with bleeding tendency and was found to have factor VIII abnormality (mammography was performed to search for primary breast carcinoma), one presented with left breast enlargement with left axillary mass, one presented with right axillary mass, and 12 presented with palpable breast mass(es). Mammographic breast density was extremely dense in five, heterogeneously dense in eight, scattered fibroglandular density in three, and fatty in one. Four patients had bilateral breast carcinoma and one had multicentricity. The carcinoma was correctly detected on initial mammographic evaluation in 15 patients (93.75%). The most common mammographic finding was architectural distortion (8/16 = 50%). The most common US finding was irregular hypoechoic mass (15/18 = 83.3%). There were 18 tumours in 16 patients. Mammography detected 16 tumours but US detected 18 tumours. US was not better than mammography in the detection of tumours but was helpful in the detection of multicentricity and guide biopsy.

Conclusion: The most common mammographic feature of ILC was architectural distortion and the most common US feature of ILC was irregular or ill-defined hypoechoic mass with acoustic shadowing. These findings were similar to other studies. The rate of missed diagnosis was not high but this is likely because most of our patients were symptomatic. US was not helpful to improve detection of ILC but was helpful to confirm the suspicious abnormalities on mammograms, detect multicentricity and guide biopsy. � 2010 Biomedical Imaging and Intervention Journal. All rights reserved.

Keywords: breast neoplasms, diagnosis, invasive lobular carcinoma

Introduction

Breast carcinoma is a histologically heterogeneous disease. Invasive lobular carcinoma (ILC) is the second most common breast malignancy after invasive ductal carcinoma (IDC), accounting for 1% to 20% of all breast cancers [1]. This wide variation reflects different diagnostic criteria and the inclusion of variant forms of the cancer. However, most studies suggest that approximately 7-10% of all invasive breast cancers are ILC [2-4]. At histopathology, ILC is typically composed of uniform small cells that diffusely infiltrate in linear fashion (single file) with scarce fibrotic reaction [5] leading to difficulty in diagnosis either by clinical examination or mammography [1,2]. ILC also has a higher rate of mammographically false-negative results [6,7]. Because mammography has limitation in detecting ILC, other imaging modalities such as ultrasonography (US) and magnetic resonance imaging (MRI) have been introduced to improve diagnostic sensitivity in patients with clinically suspicious lesions [4, 8-13]. This study was undertaken to review the mammographic and US findings of ILC at the authors� institution, determine the role of US in the detection of ILC, and determine if ILC is frequently missed on mammography.

Materials and Methods

The study was approved by the Institutional Review Board. Between January 2000 and July 2008, medical records and pathological diagnosis of 1,146 invasive breast carcinomas at the authors� institution were retrospectively reviewed. Only patients with pathologically-proven pure ILC were included. Patients with mixed lesions, containing both ILC and ductal carcinoma were excluded. Mammography was performed using dedicated film-screen equipments (LoRAD MIII: Damburg, Conn, USA, Siemens Mammomat 3000 Nova, Germany) and the Fuji Computed Radiography System (Fuji Corporation, Tokyo, Japan). Images were obtained in two standard views [mediolateral oblique (MLO) and craniocaudal (CC)], with additional views as deemed necessary. US was obtained using a variety of commercially available 5-14 MHz transducers (HDI 5000, Advanced Technology Laboratories, Bothell, WA, USA, Siemens, Sequoia, Acuson, CA, USA, Toshiba Nemio XG, SSA-580A, Japan and Toshiba Aplio XG, Japan). The initial mammographic reports were analysed to determine the true-positive and false-negative rates for the detection of cancer. Mammographic images were retrospectively reevaluated by two breast radiologists with knowledge of the pathologic report to determine the presence of focal mass, the shape, margin and density of mass, calcification, architectural distortion, asymmetrical density, axillary lymphadenopathy and associated features such as skin thickening, nipple retraction, and breast oedema. In the authors� practice, US was additionally performed in patients with dense breasts and patients with suspicious findings on mammogram to confirm the presence of a lesion. If the lesion was nonpalpable, US was used to guide biopsy since US guided-biopsy is easier, less expensive and avoided radiation compared to mammogram. US images were assessed for the presence of mass, shape, margins, echo pattern, orientation, posterior acoustic feature, and calcification. Agreement on the imaging findings was by consensus. The mammographic and US findings were determined according to the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) lexicon [14]. Pathologic review of all lesions was determined by two pathologists.�����������

Results

There were 37 patients diagnosed as pure ILC which accounted for 3% of all invasive breast carcinoma. Of the 37 patients, 16 had imaging studies and constituted the material of this study. The patients ranged in age from 45-76 years (mean age, 56.43 years). Of the 16 patients, one was asymptomatic (Figure 1), one presented with bleeding tendency and was found to have factor VIII abnormality (mammography was performed to search for primary breast carcinoma) (Figure 2), one presented with left breast enlargement and left axillary mass (Figure 3), one presented with right axillary mass, and 12 presented with palpable breast mass(es) (Figure 4). Of the 12 patients who presented with breast mass(es), one was found to have IDC on the palpable mass and ILC in the other side which was nonpalpable (Figure 5). The other 11 patients were found to have ILC at the palpable sites. Mastectomy was performed in 13 patients, breast conservative treatment (BCT) was performed in two, and one refused further treatment after core biopsy.

Mammographic breast density was extremely dense in four, heterogeneously dense in eight, scattered fibroglandular density in three, and fatty breast in one. Four patients had bilateral breast carcinoma. Of these four patients, three were metachronous and one was synchronous bilateral breast carcinoma. The first carcinoma was IDC in three and ILC in one. The carcinoma was correctly detected on initial mammographic evaluation in 15 patients (93.75%). The missed diagnostic mammogram was retrospectively seen as area of distortion on both CC and MLO (Figure 6). Multifocal lesions were detected on US in one (Figure 7). Therefore, 18 tumours were found in 16 patients. The tumour was more obviously seen on CC view than MLO view (Figures 1 and 5) in four. The most common mammographic finding was architectural distortion (8/16 = 50%) (Figures 1, 6, 8). The most common US finding was an irregular hypoechoic mass with ill-defined margins. Tables 1 and 2 summarise the mammographic and US features of ILC. US was not better than mammography in the detection of tumours but was helpful in the detection of multifocality and in guiding biopsy.����

Discussion

Of the different histological types of breast carcinoma, ILC may be the most difficult to diagnose by mammography because it characteristically spreads by a single-file infiltration of malignant cells through the breast stroma with relative paucity of connective tissue reaction, haemorrhage, necrosis, or calcifications [1, 2, 5, 15]. At mammography, ILC has a variety of appearances including mass with spiculation, ill-defined or well-defined margins, asymmetrical density, architectural distortion, microcalcifications, and normal or benign findings [2, 7, 13, 16]. According to Hilleren et al. and Lopez et al. [2, 13], the two most frequent findings were spiculated mass and architectural distortion. In our study, architectural distortion was the most common finding (50%) and ill-defined mass was the second most common (25%). Calcifications are often the earliest manifestation of ductal carcinoma but are less frequent in ILC. Calcifications were seen in only 2% in the series of Hilleren et al. [2], 4% in the series of Helvie et al. [16], and 24% in the series of Le Gal et al. [7]. In our study, 31.25% had associated calcifications. The less frequent calcifications in the series from Hilleren and Helvie may possibly be due to the poorer quality of the older mammographic machine. Bilaterality and multicentricity are characteristic features of ILC [1, 2, 5, 15, 17]. Synchronous or metachronous bilateral carcinoma occurs in up to one-third of patients with ILC [5, 16, 17]. Lobular carcinoma is common in the contralateral breast but some are ductal [17]. We found four bilateral carcinomas which was one-fourth of the patients. The contralateral carcinomas in our patients were ductal more than lobular (3:1). Multicentricity was encountered in only one and the additional tumours were detected from US. However, the true incidence of multicentricity is unknown because two had BCT and one was diagnosed by core biopsy, therefore the entire breast was not sectioned for histologic study. MRI was also not preformed in this study. The major limitation of using MRI in the authors� institution is its high cost and long waiting list.

Approximately 20% of ILC are better visualised in one mammographic view [18]. In the two series [2,19], ILC was better visualised in the CC view. In this study, four were better seen on CC view than MLO view.

The rate of false-negative findings has been reported to be as high as 43% [2, 3, 6, 7]. The high false-negative rate may be due to low opacity with poor margination of the tumour, indirect mammographic signs of malignancy (architectural distortion, asymmetrical density), and one view visualisation. The difficulty of making a diagnosis of ILC probably explains why ILC accounts for a disproportionately large percentage of potential malpractice suits investigated for failure to diagnose breast cancer [6]. In this study, only one was initially a missed diagnosis (Figure 6). The low rate of missed diagnosis in this study may be because most patients were symptomatic. In a true population-based screening programme or in asymptomatic individuals, it would be more difficult when there is no �clue� as to the presence of a lesion.

Because of the limitations of mammography in detecting ILC, US and MRI have been used to improve the diagnosis of ILC and to assess the extent of disease in known cancers [4, 8-13, 20,2 1]. Paramagul et al [8] concluded in their study that US was not sensitive and nonspecific in the diagnosis of ILC but more recent studies showed that US is a useful adjunct to mammography in the evaluation of ILC [4, 9, 12]. In this study, additional US was performed in all 16 patients, even in fatty and scattered fibroglandular breasts, to confirm if there was abnormality over the mammographic suspicious findings. If the lesion was nonpalpable, US guided-biopsy was used since it was easier, less expensive and produced no radiation. In this study, the most common US feature was an irregular hypoechoic mass with acoustic shadowing which was similar to other studies [4, 8, 9, 12]. Cawson et al. [9] also found atypical US feature of hyperechoic mass and a wider than tall appearance. In this study, one hyperechoic mass was found but it was different from that found in Cawson et al. The tumour in this study was totally hyperechoic but in their study tumours were centrally hypoechoic with peripheral hyperechoic. One patient who had synchronous bilateral breast carcinoma presented with a palpable mass on the left side and was found to have IDC. Mammogram of the right breast showed architectural distortion which was seen only on the CC view. US showed an area of ill-defined heterogeneous echo and biopsy was performed using US guide which showed ILC. US could not demonstrate abnormality in one patient who was initially a missed diagnosis. Retrospectively reviewed mammograms demonstrated an area of architectural distortion which might show as an abnormality on US if the first reader did not miss the lesion. Though supplemental US after mammography can increase the rate of breast cancer detection, it should be performed by specially trained radiologists since breast US is highly operator-dependent [22, 23]. Though it seems that US did not improve detection of ILC in this study, it was helpful to confirm the suspicious lesions from mammography, detect multicentricity, and guide biopsy.

MRI has been introduced as a useful adjunct to mammography and US in the detection and assessment of the size of ILC [10, 11, 13, 20, 21]. Mann et al. found that MRI was able to detect additional ipsilateral and contralateral malignant findings not evident at mammography or US in patients with ILC [20]. Because re-excision rates after breast-conserving surgery (BCS) of ILC are high, preoperative breast MRI has been proven to reduce re-excision rates without increasing the rates of mastectomies [21]. However, MRI was not performed in this study because of its high cost and long waiting list.

In conclusion, the most common mammographic features of ILC was architectural distortion and the most common US feature of ILC was an irregular or ill-defined hypoechoic mass with acoustic shadowing. These findings were similar to other studies. The rate of missed diagnosis is not high but this is likely because most of the patients in this study were symptomatic. US was not helpful to improve detection of ILC but was helpful to confirm the suspicious abnormalities on mammograms, detect multicentricity, and guide biopsy.

Figure 1 Metachronous bilateral breast carcinomas. A 54-year-old woman who had history of right mastectomy for IDC 2 years ago came for mammographic screening of the left breast. (A) Left MLO and (B) CC mammograms show an area of mild architectural distortion (arrow) at the outer quadrant which is seen only from CC view. (C) US at the outer quadrant of the left breast shows an irregular hypoechoic mass with acoustic shadowing which proved to be ILC. BCT was performed. (D) Photomicrograph shows slightly large tumour cells arranged in cords and single rows. Mitotic figures are rarely seen (H&E; stain, x400).

Figure 2 A 74-year-old woman presented with bleeding tendency and was found to have factor VIII abnormality, mammography was performed to search for primary breast cancer. (A) Bilateral MLO mammograms show fatty breasts with ill-defined mass (arrow) in the left upper breast. (B) US image of the left breast mass shows an ill-defined high echogenic mass (arrows) with mild acoustic shadowing.

Figure 3 A 62-year-old woman presented with left breast enlargement and a palpable left axillary mass. (A) Bilateral MLO mammograms show heterogeneous dense breasts with diffuse increased breast density and coarse trabeculation on the left side. Scattered micro and macrocalcifications are also seen in the left breast with thickening of the overlying skin. There are multiple enlarged left axillary lymph nodes with increased density and loss of fatty hilum. (B) US of the left breast shows irregular low echogenic mass with calcifications (arrow) and skin thickening.

Figure 4 A 52-year-old woman presented with left breast mass and skin retraction. (A) and (B) Bilateral MLO and CC show a 1.5 cm spiculated mass with faint microcalcifications in the left upper outer quadrant. Skin thickening with retraction (arrow) is shown in the left CC mammogram.

Figure 5 Synchronous bilateral breast carcinomas, ILC on the right side and IDC on the left side. A 56-year-old woman presented with a palpable left breast mass. (A) and (B) Bilateral MLO and CC mammograms show an ill-defined mass at the left upper outer quadrant (arrowheads) which proved to be IDC. There is an area of architectural distortion at the inner quadrant of the left breast seen on CC view (arrow) but no definite distortion or mass on the MLO view. US on the right inner quadrant showed an area of ill-defined heterogeneous echo (not shown) and biopsy was done by US guided which showed ILC.

Figure 6 Metachronous bilateral invasive lobular carcinoma. A 52-year-old woman who was a known case of ILC with left mastectomy one year ago presented with a palpable right axillary mass. The initial mammography was reported as right axillary nodal metastasis without lesion in the right breast. (A) and (B) Bilateral MLO and CC mammograms shows an area of architectural distortion at the upper outer quadrant (arrow). The right axillary node is enlarged and has increased density with loss of fatty hilum. Physical re-examination by the surgeon found a thickening area in the right upper outer quadrant. Biopsy revealed invasive lobular carcinoma.

Figure 7 A 53-year-old woman presented with a palpable right breast mass. (A) Bilateral MLO mammograms show an ill-defined mass with microcalcifications at the right upper outer quadrant (arrow). (B) Composite US images at the right upper outer quadrant show three irregular low echogenic masses with calcifications in the big mass (arrow).

Figure 8 ILC seen as architectural distortion. A 54-year-old woman presented with a palpable mass on the right upper outer quadrant. (A) and (B) Bilateral MLO and CC mammograms show area of architectural distortion at the right upper outer quadrant.

Table 1 Mammographic findings of 16 patients

Table 2 US findings of 18 tumours in 16 patients

References

  1. Yeh C, Titus JM, Kalisher L. Breast imaging case of the day. Infiltrating lobular carcinoma (ILC). Radiographics 1997; 17(5):1328-32.   [Medline]
  2. Hilleren DJ, Andersson IT, Lindholm K et al. Invasive lobular carcinoma: mammographic findings in a 10-year experience. Radiology 1991; 178(1):149-54.   [Medline]
  3. Krecke KN, Gisvold JJ. Invasive lobular carcinoma of the breast: mammographic findings and extent of disease at diagnosis in 184 patients. AJR Am J Roentgenol 1993; 161(5):957-60.   [Medline]
  4. Butler RS, Venta LA, Wiley EL et al. Sonographic evaluation of infiltrating lobular carcinoma. AJR Am J Roentgenol 1999; 172(2):325-30.   [Medline]
  5. Dixon JM, Anderson TJ, Page DL et al. Infiltrating lobular carcinoma of the breast. Histopathology 1982; 6(2):149-61.   [Medline]
  6. Sickles EA. The subtle and atypical mammographic features of invasive lobular carcinoma. Radiology 1991; 178(1):25-6.   [Medline]
  7. Le Gal M, Ollivier L, Asselain B et al. Mammographic features of 455 invasive lobular carcinomas. Radiology 1992; 185(3):705-8.   [Medline]
  8. Paramagul CP, Helvie MA, Adler DD. Invasive lobular carcinoma: sonographic appearance and role of sonography in improving diagnostic sensitivity. Radiology 1995; 195(1):231-4.   [Medline]
  9. Cawson JN, Law EM, Kavanagh AM. Invasive lobular carcinoma: sonographic features of cancers detected in a BreastScreen Program. Australas Radiol 2001; 45(1):25-30.   [Medline]
  10. Qayyum A, Birdwell RL, Daniel BL et al. MR imaging features of infiltrating lobular carcinoma of the breast: histopathologic correlation. AJR Am J Roentgenol 2002; 178(5):1227-32.   [Medline]
  11. Boetes C, Veltman J, van Die L et al. The role of MRI in invasive lobular carcinoma. Breast Cancer Res Treat 2004; 86(1):31-7.   [Medline]
  12. Selinko VL, Middleton LP, Dempsey PJ. Role of sonography in diagnosing and staging invasive lobular carcinoma. J Clin Ultrasound 2004; 32(7):323-32.   [Medline]
  13. Lopez JK, Bassett LW. Invasive lobular carcinoma of the breast: spectrum of mammographic, US, and MR imaging findings. Radiographics 2009; 29(1):165-76.   [Medline]
  14. American College of the Radiology. Breast Imaging Report and Data System (BI-RADS). 4th edition. Reston, VA: American College of Radiology, 2003.  
  15. Rosen PP. The pathology of invasive breast carcinoma. In: Harris JR, Hellman S, Henderson IC et al., eds. Breast diseases. 2nd edition. Philadelphia: Lippincott, 1991: 272-6.  
  16. Helvie MA, Paramagul C, Oberman HA et al. Invasive lobular carcinoma. Imaging features and clinical detection. Invest Radiol 1993; 28(3):202-7.   [Medline]
  17. Lesser ML, Rosen PP, Kinne DW. Multicentricity and bilaterality in invasive breast carcinoma. Surgery 1982; 91(2):234-40.   [Medline]
  18. Andersson I, Hildell J, Muhlow A et al. Number of projections in mammography: influence on detection of breast disease. AJR Am J Roentgenol 1978; 130(2):349-51.   [Medline]
  19. Newstead GM, Baute PB, Toth HK. Invasive lobular and ductal carcinoma: mammographic findings and stage at diagnosis. Radiology 1992; 184(3):623-7.   [Medline]
  20. Mann RM, Hoogeveen YL, Blickman JG et al. MRI compared to conventional diagnostic work-up in the detection and evaluation of invasive lobular carcinoma of the breast: a review of existing literature. Breast Cancer Res Treat 2008; 107(1):1-14.   [Medline]
  21. Mann RM, Loo CE, Wobbes T et al. The impact of preoperative breast MRI on the re-excision rate in invasive lobular carcinoma of the breast. Breast Cancer Res Treat 2010; 119(2):415-22.   [Medline]
  22. Berg WA. Supplemental screening sonography in dense breasts. Radiol Clin North Am 2004; 42(5):845-51, vi.   [Medline]
  23. Berg WA, Blume JD, Cormack JB et al. Operator dependence of physician-performed whole-breast US: lesion detection and characterization. Radiology 2006; 241(2):355-65.   [Medline]

Received 30 December 2009; received in revised form 29 January 2010, accepted 1 February 2010

Correspondence: Department of Radiology, Chiang Mai University, Chiang Mai, Thailand. Tel.: +66 53945450; Fax: +66 53946136; E-mail: mmuttara@mail.med.cmu.ac.th (Malai Muttarak).

Please cite as: Muttarak M, Sangchan S, Kongmebhol P, Sukhamwang N, Chaiwun B, Mammographic and ultrasonographic features of invasive lobular carcinoma: a review of 16 patients, Biomed Imaging Interv J 2010; 6(3):e21
<URL: http://www.biij.org/2010/3/e21/>


University of Malaya, Kuala Lumpur, Malaysia

Sponsors

GE
Bayer Healthcare
Siemens
Agfa
Toshiba
Philips
Elekta Fujifilm Barco Transmedic

Official publication of

ASEAN Association of Radiologists
ASEAN Society of Interventional Radiology
Asia-Oceania Federation of Organizations for Medical Physics
Asian Oceania Society of Radiology
College of Radiology, Academy of Medicine Malaysia
Southeast Asian Federation of Organisations of Medical Physics
South East Asian Association of Academic Radiologists

Published by

Department of Biomedical Imaging, Faculty of Medicine, University of Malaya, Malaysia




   

Biomedical Imaging and Intervention Journal. ISSN 1823-5530 RSS | Facebook | Twitter


 
   
Creative Commons License
Except where otherwise noted, articles published in the Biomedical Imaging and Intervention Journal
are distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited, including full bibliographic details and the URL, and this statement is included.