Abstract
The aim of our study was to assess the performance of contrast-enhanced digital mammography (CEDM) in the preoperative loco-regional staging of invasive lobular carcinoma (ILC) patients, about the valuation of the extension of disease and in measurement of lesions. Then, we selected retrospectively, among the 1500 patients underwent to CEDM at the Breast Diagnostics Department of the Careggi University Hospital of Florence and the National Cancer Institute of Milan from September 2016 to November 2018, 31 women (mean age 57.1 aa; range 41–78 aa) with a definitive histological diagnosis of ILC. CEDM has proved to be a promising imaging technique, being characterized by a sensitivity of 100% in the detection of the index lesion, and of 84.2% in identifying any adjunctive lesions: It was the presence of a non-mass enhancement (NME) to lower the sensitivity of the technique (25% vs. 100% for mass-like enhancements or a mass closely associated with a NME). Specificity in the characterization of additional lesions was 66.7%, and the diagnosis of the extension of disease was correct in 77.4% of cases: NME also led to a decrease in diagnostic accuracy in the evaluation of disease extension up to 40% versus 85% for masses and 80% for masses associated with NME (M/NME). Moreover, in 12/31 (38.7%), CEDM allowed to correctly identify lesions not shown by mammography + ultrasonography + tomosynthesis: In the half of these (6/12), there was a multicentricity, thus allowing an adequate surgical planning change. CEDM was also very accurate in analyzing the maximum diameter of the masses, while it was much less reliable in the case of the M/NME and pure NME. In conclusion, CEDM is a new promising imaging technique in the loco-regional preoperative staging and in the evaluation of disease extension for ILC, especially in case of mass enhancement lesions.
Similar content being viewed by others
References
Li CI, Anderson BO, Daling JR, Moe RE (2003) Trends in incidence rates of invasive lobular and ductal breast carcinoma. JAMA 289:1421–1424
Arpino G, Bardou VJ, Clark GM, Elledge RM (2004) Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 6:R149–R156
Macchini M, Ponziani M, Iamurri AP et al (2018) Role of DCE-MR in predicting breast cancer subtypes. Radiol Med 123(10):753–764
Berg WA, Gutierrez L, NessAiver MS et al (2004) Diagnostic accuracy of mammography, clinical examination, US, and MR imaging in preoperative assessment of breast cancer. Radiology 233:830–849
Brem RF, Ioffe M, Rapelyea JA et al (2009) Invasive lobular carcinoma: detection with mammography, sonography, MRI, and breast- specific gamma. AJR Am J Roentgenol 192:379–383
Butler RS, Venta LA, Wiley EL, Ellis RL, Dempsey PJ, Rubin E (1999) Sonographic evaluation of infiltrating lobular carcinoma. AJR Am J Roentgenol 172:325–330
Montemezzi S, Cavedon C, Camera L et al (2017) 1H-MR spectroscopy of suspicious breast mass lesions at 3T: a clinical experience. Radiol Med 122(3):161–170
Weinstein SP, Orel SG, Heller R et al (2001) MR Imaging of the breast in patients with invasive lobular carcinoma. AJR Am J Roentgenol 176:399–406
Zanotel M, Bednarova I, Londero V et al (2018) Automated breast ultrasound: basic principles and emerging clinical applications. Radiol Med 123(1):1–12
Mann RM, Hoogeveen YL, Blickman JG, Boetes C (2008) 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 107:1–14
Selvi V, Nori J, Meattini I, Francolini G, Morelli N, De Benedetto D, Bicchierai G, Di Naro F, Gill MK, Orzalesi L, Sanchez L, Susini T, Bianchi S, Livi L, Miele V (2018) Role of magnetic resonance imaging in the preoperative staging and work-up of patients affected by invasive lobular carcinoma or invasive ductolobular carcinoma. Biomed Res Int. https://doi.org/10.1155/2018/1569060
ACR Guidelines and Standards Committee (2008) ACR practice guideline for the performance of contrast-enhanced magnetic resonance imaging (MRI) of the breast
Kalovidouri A, Firmenich N, Delattre BMA et al (2017) Fat suppression techniques for breast MRI: Dixon versus spectral fat saturation for 3D T1-weighted at 3 T. Radiol Med 122(10):731–742
Mann RM, Kuhl CK, Kinkel K, Boetes C (2008) Breast MRI: guidelines from the European Society of Breast Imaging. Eur Radiol 18:1307–1318
Lee-Felker Stephanie A et al (2017) Newly diagnosed breast cancer: comparison of contrast-enhanced spectral mammography and breast mr imaging in the evaluation of extent of disease. Radiology 285(2):389–400
Jochelson MS, Dershaw DD, Sung JS et al (2013) Bilateral contrast-enhanced dual-energy digital mammography: feasibility and comparison with conventional digital mammography and MR imaging in women with known breast carcinoma. Radiology 266:743–751
Hobbs MM, Taylor DB, Buzynski S, Peake RE (2015) Contrast-enhanced spectral mammography (CESM) and contrast enhanced MRI (CEMRI): patient preferences and tolerance. J Med Imaging Radiat Oncol 59:300–305
Bernardi D, Belli P, Benelli E et al (2017) Digital breast tomosynthesis (DBT): recommendations from the Italian College of BreastRadiologists (ICBR) by the Italian Society of Medical Radiology (SIRM) and the Italian Group for Mammography Screening (GISMa). Radiol Med 122(10):723–730
Patel BK, Gray RJ, Pockaj BA (2017) Potential cost savings of contrast-enhanced digital mammography. AJR Am J Roentgenol 5:1–7. https://doi.org/10.2214/AJR.16.17239
Luczynska E, Heinze-Paluchowska S, Hendrick E et al (2015) Comparison between breast MRI and contrast-enhanced spectral mammography. Med Sci Monit 21:1358–1367
Francescone MA, Jochelson MS, Dershaw DD, Sung JS, Hughes MC, Zheng J, Moskowitz C, Morris EA (2014) Low energy mammogram obtained in contrast-enhanced digital mammography (CEDM) is comparable to routine full-field digital mammography (FFDM). Eur J Radiol 83(8):1350–1355
Bicchierai G, Nori J, De Benedetto D, Boeri C, Vanzi E, Bianchi S, Kaur Gill M, Cirone D, Miele V (2018) Role of contrast-enhanced spectral mammography in the post biopsy management of B3 lesions: preliminary results. Tumori J 17:300891618816212
Trimboli RM, Codari M, Khouri Chalouhi K et al (2018) Correlation between voxel-wise enhancement parameters on DCE-MRI and pathologicalprognostic factors in invasive breast cancers. Radiol Med 123(2):91–97
Bicchierai G, Di Naro F, Amato F (2018) CEDM lexicon and imaging interpretation tips. In: Nori J, Kaur M (eds) Contrast-enhanced digital mammography (CEDM), chapter. 9; pp 93–118. Springer, Berlin. ISBN 978-3-319- 94552-1. eBook ISBN 978-3-319-94553-8. https://doi.org/10.1007/978-3-319-94553-8_9
D’Orsi CJACR (2013) BI-RADS atlas: breast imaging reporting and data system. American College of Radiology, Reston
Morris EA, Comstock CE, Lee CH et al (2013) ACR BI-RADS® magnetic resonance imaging. In: ACR BI-RADS® Atlas, Breast imaging reporting and data system. American College of Radiology, Reston
Bartolotta TV, Orlando A, Cantisani V et al (2018) Focal breast lesion characterization according to the BI-RADS US lexicon: role of a computer-aided decision-making support. Radiol Med 123(7):498–506
Hilleren DJ, Andersson IT, Lindholm K, Linnell FS (1991) Invasive lobular carcinoma: mammographic findings in a 10-year experience. Radiology 178:149–154
Krecke KN, Gisvold JJ (1993) Invasive lobular carcinoma of the breast: mammographic findings and extent of disease at diagnosis in 184 patients. AJR Am J Roentgenol 161:957–960
Le Gal M, Ollivier L, Asselain B, Meunier M, Laurent M, Vielh P (1992) Mammographic features of 455 invasive lobular carcinomas. Radiology 185:705–708
Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1(8476):307–310
Koo Terry K, Li Mae Y (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15(2):155–163. https://doi.org/10.1016/j.jcm.2016.02.012
Lee-Felker SA et al (2017) Newly diagnosed breast cancer: comparison of contrast-enhanced spectral mammography and breast MR imaging in the evaluation of extent of disease. Radiology 285(1):389–400
Boetes C et al (1995) Breast tumors: comparative accuracy of MR imaging relative to mammography and US for demonstrating extent. Radiology 197(3):743–747
Schelfout K et al (2004) Preoperative breast MRI in patients with invasive lobular breast cancer. Eur Radiol 14(7):1209–1216
Carin Anne-julie, Molière Sébastien, Gabriele Victor, Lodi Massimo, Thiébaut Nicolas, Neuberger Karl, Mathelin Carole (2017) Relevance of breast MRI in determining the size and focality of invasive breast cancer treated by mastectomy: a prospective study. World J Surg Oncol 15:128. https://doi.org/10.1186/s12957-017-1197-1
Marino MA, Pennisi O, Donia A et al (2017) Organizational and welfare mode of breast centers network: a survey of Sicilian radiologists. Radiol Med 122(9):639–650
Gruber IV et al (2013) Measurement of tumour size with mammography, sonography and magnetic resonance imaging as compared to histological tumour size in primary breast cancer. BMC Cancer 13(1):328
Kneeshaw PJ, Turnbull LW, Smith A, Drew PJ (2003) Dynamic contrast enhanced magnetic resonance imaging aids the surgical management of invasive lobular breast cancer. Eur J Surg Oncol 29(1):32–37
Rodenko GN, Harms SE, Pruneda JM, Farrell RS Jr, Evans WP, Copit DS, Krakos PA, Flamig DP (1996) MR imaging in the management before surgery of lobular carcinoma of the breast: correlation with pathology. AJR Am J Roentgenol 167(6):1415–1419
Patel BK, Davis J, Ferraro C, Kosiorek H, Hasselbach K, Ocal T, Pockaj B (2018) Value added of preoperative contrast enhanced digital mammography in patients with invasive lobular carcinoma of the breast. Clin Breast Cancer. https://doi.org/10.1016/j.clbc.2018.07.012
Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thürlimann B, Senn H-J (2013) Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol 24(9):2206–2223
Jiang Yi-Zhou, Xia Chen, Peng Wen-Ting, Ke-Da Yu, Zhuang Zhi-Gang, Shao Zhi-Ming (2014) Preoperative measurement of breast cancer overestimates tumor size compared to pathological measurement. PLoS ONE 9(1):e86676. https://doi.org/10.1371/journal.pone.0086676
Fallenberg EM, Dromain C, Diekmann F et al (2014) Contrast-enhanced spectral mammography versus MRI: initial results in the detection of breast cancer and assessment of tumour size. Eur Radiol 24:256–264
Zheng Y, Zhong M, Ni C et al (2017) Radiotherapy and nipple-areolar complex necrosis after nipple-sparing mastectomy: asystematic review and meta-analysis. Radiol Med 122(3):171–178
Kanyilmaz G, Aktan M, Koc M et al (2017) Unplanned irradiation of internal mammary lymph nodes in breast cancer. Radiol Med 122(6):405–411
Thomas M, Kelly ED, Abraham J et al (2019) Invasive lobular breast cancer: a review of pathogenesis, diagnosis, management, and future directions of early stage disease. Semin Oncol 46(2):121–132
Fiorentino A, Mazzola R, Naccarato S et al (2017) Synchronous bilateral breast cancer irradiation: clinical and dosimetrical issues using volumetricmodulated arc therapy and simultaneous integrated boost. Radiol Med 122(6):464–471
Iorfida Monica, Maiorano Eugenio, Orvieto Enrico, Maisonneuve Patrick, Bottiglieri Luca, Rotmensz Nicole, Montagna Emilia, Dellapasqua Silvia, Veronesi Paolo, Galimberti Viviana, Luini Alberto, Goldhirsch Aaron, Colleoni Marco, Viale Giuseppe (2012) Invasive lobular breast cancer: subtypes and outcome. Breast Cancer Res Treat 133:713–723. https://doi.org/10.1007/s10549-012-2002-z
Fallahpour S, Navaneelan T, De P, Borgo A (2017) Breast cancer survival by molecular subtype: a population-based analysis of cancer registry data. CMAJ Open 5:E734–E739
Funding
None.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee: “Regione Toscana, Comitato Etico Area Vasta Centro, reference number: SPE_16.251” and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Ethical standards
This article does not contain any studies with animals performed by any of the authors.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Amato, F., Bicchierai, G., Cirone, D. et al. Preoperative loco-regional staging of invasive lobular carcinoma with contrast-enhanced digital mammography (CEDM). Radiol med 124, 1229–1237 (2019). https://doi.org/10.1007/s11547-019-01116-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11547-019-01116-7