Skip to main content
Top
Published in: La radiologia medica 10/2015

01-10-2015 | BREAST RADIOLOGY

MR mammography using diffusion-weighted imaging in evaluating breast cancer: a correlation with proliferation index

Authors: Cristina Molinari, Paola Clauser, Rossano Girometti, Anna Linda, Elisa Cimino, Fabio Puglisi, Chiara Zuiani, Massimo Bazzocchi

Published in: La radiologia medica | Issue 10/2015

Login to get access

Abstract

Purpose

To evaluate whether the variation of the apparent diffusion coefficient (ADC) values obtained with DWI can predict elevated levels of Ki67 proliferation index and aggressive subtypes in patients with breast cancer.

Materials and methods

Breast MRI studies of 115 patients (mean age 57.3 years, range 36–81 years) with a biopsy-proven breast cancers were evaluated in this retrospective IRB-approved study. Examinations were performed on a 1.5 T magnet and included a Single-Shot Echoplanar DWI sequence with b values of 0 and 1000 s/mm2. For each target lesion, ADC was measured. ADC values were compared considering Ki67 status (≥20 % or <20 %), histology, grade (G1, G2 or G3) and clinical–pathological classification (Luminal A, Luminal B HER2-positive, Luminal B HER-2 negative, HER-2 enriched and Triple Negative). Mann–Whitney U test and Kruskal–Wallis test were used for comparisons and receiver operating characteristic (ROC) curves were obtained. Inter- and intra-reader variability was evaluated in a subset of 40 patients, using interclass correlation coefficient (ICC) and Bland–Altman plots.

Results

Of 115 lesions, 53 (46.1 %) were assessed as Ki67 positive and 62 (53.9 %) as Ki67 negative. ADC values were significantly (p < 0.0001) lower in Ki67-positive patients (median 0.86 × 10−3 mm2/s; interquartile range 0.75–0.92) compared to Ki67-negative (median 1.03 × 10−3 mm2/s; interquartile range 0.92–1.13). Median ADC was also lower in G2 and G3 cancer and in the Luminal B Her2-negative subtype (p = 0.0015). No differences were found when evaluating histology. ROC curve showed a sensitivity and specificity of 83.0 and 66.1 %, respectively, when using a cutoff of 0.95 s/mm2 to differentiate Ki67-positive from Ki67-negative cancers. Inter- and intra-reader variability was moderate (ICC = 0.623; ICC = 0.548, respectively). No systematic differences were identified with Bland–Altman plots.

Conclusions

Lower ADC values are associated with elevated Ki67 proliferation index and more aggressive pathologic features. Moderate agreement in ADC measurement could be a limitation.
Literature
1.
go back to reference Lakhani SR, Ellis IO, Schnitt SJ, et al. (2012) WHO classification of tumours, Volume 4 IARC WHO classification of tumours, No 4, IARC. Lyon Lakhani SR, Ellis IO, Schnitt SJ, et al. (2012) WHO classification of tumours, Volume 4 IARC WHO classification of tumours, No 4, IARC. Lyon
3.
5.
go back to reference Houssami N, Ciatto S, Macaskill P et al (2008) Accuracy and surgical impact of magnetic resonance imaging in breast cancer staging: systematic review and meta-analysis in detection of multifocal and multicentric cancer. J Clin Oncol 26:3248–3258. doi:10.1200/JCO.2007.15.2108 CrossRefPubMed Houssami N, Ciatto S, Macaskill P et al (2008) Accuracy and surgical impact of magnetic resonance imaging in breast cancer staging: systematic review and meta-analysis in detection of multifocal and multicentric cancer. J Clin Oncol 26:3248–3258. doi:10.​1200/​JCO.​2007.​15.​2108 CrossRefPubMed
6.
go back to reference Benndorf M, Baltzer PAT, Vag T et al (2010) Breast MRI as an adjunct to mammography: does it really suffer from low specificity? A retrospective analysis stratified by mammographic BI-RADS classes. Acta Radiol Stockh Swed 51:715–721. doi:10.3109/02841851.2010.497164 Benndorf M, Baltzer PAT, Vag T et al (2010) Breast MRI as an adjunct to mammography: does it really suffer from low specificity? A retrospective analysis stratified by mammographic BI-RADS classes. Acta Radiol Stockh Swed 51:715–721. doi:10.​3109/​02841851.​2010.​497164
9.
go back to reference Tsushima Y, Takahashi-Taketomi A, Endo K (2009) Magnetic resonance (MR) differential diagnosis of breast tumors using apparent diffusion coefficient (ADC) on 1.5-T. J Magn Reson Imaging 30:249–255. doi:10.1002/jmri.21854 CrossRefPubMed Tsushima Y, Takahashi-Taketomi A, Endo K (2009) Magnetic resonance (MR) differential diagnosis of breast tumors using apparent diffusion coefficient (ADC) on 1.5-T. J Magn Reson Imaging 30:249–255. doi:10.​1002/​jmri.​21854 CrossRefPubMed
10.
go back to reference Kinoshita T, Yashiro N, Ihara N et al (2002) Diffusion-weighted half-Fourier single-shot turbo spin echo imaging in breast tumors: differentiation of invasive ductal carcinoma from fibroadenoma. J Comput Assist Tomogr 26:1042–1046CrossRefPubMed Kinoshita T, Yashiro N, Ihara N et al (2002) Diffusion-weighted half-Fourier single-shot turbo spin echo imaging in breast tumors: differentiation of invasive ductal carcinoma from fibroadenoma. J Comput Assist Tomogr 26:1042–1046CrossRefPubMed
12.
go back to reference Dorrius MD, Dijkstra H, Oudkerk M, Sijens PE (2014) Effect of b value and pre-admission of contrast on diagnostic accuracy of 1.5-T breast DWI: a systematic review and meta-analysis. Eur Radiol 24:2835–2847. doi:10.1007/s00330-014-3338-z CrossRefPubMed Dorrius MD, Dijkstra H, Oudkerk M, Sijens PE (2014) Effect of b value and pre-admission of contrast on diagnostic accuracy of 1.5-T breast DWI: a systematic review and meta-analysis. Eur Radiol 24:2835–2847. doi:10.​1007/​s00330-014-3338-z CrossRefPubMed
13.
go back to reference Li X-R, Cheng L-Q, Liu M et al (2012) DW-MRI ADC values can predict treatment response in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy. Med Oncol Northwood Lond Engl 29:425–431. doi:10.1007/s12032-011-9842-y CrossRef Li X-R, Cheng L-Q, Liu M et al (2012) DW-MRI ADC values can predict treatment response in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy. Med Oncol Northwood Lond Engl 29:425–431. doi:10.​1007/​s12032-011-9842-y CrossRef
15.
go back to reference Elston CW, Ellis IO (1991) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 19:403–410CrossRefPubMed Elston CW, Ellis IO (1991) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 19:403–410CrossRefPubMed
16.
go back to reference Wolff AC, Hammond MEH, Schwartz JN et al (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol Off J Am Soc Clin Oncol 25:118–145. doi:10.1200/JCO.2006.09.2775 CrossRef Wolff AC, Hammond MEH, Schwartz JN et al (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol Off J Am Soc Clin Oncol 25:118–145. doi:10.​1200/​JCO.​2006.​09.​2775 CrossRef
17.
go back to reference Kuroki Y, Nasu K, Kuroki S et al (2004) Diffusion-weighted imaging of breast cancer with the sensitivity encoding technique: analysis of the apparent diffusion coefficient value. Magn Reson Med Sci 3:79–85. doi:10.2463/mrms.3.79 CrossRefPubMed Kuroki Y, Nasu K, Kuroki S et al (2004) Diffusion-weighted imaging of breast cancer with the sensitivity encoding technique: analysis of the apparent diffusion coefficient value. Magn Reson Med Sci 3:79–85. doi:10.​2463/​mrms.​3.​79 CrossRefPubMed
20.
go back to reference Dowsett M, Nielsen TO, A’Hern R et al (2011) Assessment of Ki67 in Breast cancer: recommendations from the International Ki67 in Breast Cancer Working Group. JNCI J Natl Cancer Inst 103:1656–1664. doi:10.1093/jnci/djr393 CrossRefPubMed Dowsett M, Nielsen TO, A’Hern R et al (2011) Assessment of Ki67 in Breast cancer: recommendations from the International Ki67 in Breast Cancer Working Group. JNCI J Natl Cancer Inst 103:1656–1664. doi:10.​1093/​jnci/​djr393 CrossRefPubMed
22.
go back to reference Jansen RL, Hupperets PS, Arends JW et al (1998) MIB-1 labelling index is an independent prognostic marker in primary breast cancer. Br J Cancer 78:460–465CrossRefPubMedPubMedCentral Jansen RL, Hupperets PS, Arends JW et al (1998) MIB-1 labelling index is an independent prognostic marker in primary breast cancer. Br J Cancer 78:460–465CrossRefPubMedPubMedCentral
23.
24.
go back to reference Muraoka N, Uematsu H, Kimura H et al (2008) Apparent diffusion coefficient in pancreatic cancer: characterization and histopathological correlations. J Magn Reson Imaging JMRI 27:1302–1308. doi:10.1002/jmri.21340 CrossRefPubMed Muraoka N, Uematsu H, Kimura H et al (2008) Apparent diffusion coefficient in pancreatic cancer: characterization and histopathological correlations. J Magn Reson Imaging JMRI 27:1302–1308. doi:10.​1002/​jmri.​21340 CrossRefPubMed
25.
go back to reference Rosenkrantz AB, Niver BE, Fitzgerald EF et al (2010) Utility of the apparent diffusion coefficient for distinguishing clear cell renal cell carcinoma of low and high nuclear grade. Am J Roentgenol 195:W344–W351. doi:10.2214/AJR.10.4688 CrossRef Rosenkrantz AB, Niver BE, Fitzgerald EF et al (2010) Utility of the apparent diffusion coefficient for distinguishing clear cell renal cell carcinoma of low and high nuclear grade. Am J Roentgenol 195:W344–W351. doi:10.​2214/​AJR.​10.​4688 CrossRef
27.
go back to reference Onishi N, Kanao S, Kataoka M et al (2014) Apparent diffusion coefficient as a potential surrogate marker for Ki-67 index in mucinous breast carcinoma. J Magn Reson Imaging JMRI. doi:10.1002/jmri.24615 Onishi N, Kanao S, Kataoka M et al (2014) Apparent diffusion coefficient as a potential surrogate marker for Ki-67 index in mucinous breast carcinoma. J Magn Reson Imaging JMRI. doi:10.​1002/​jmri.​24615
28.
go back to reference Jeh SK, Kim SH, Kim HS et al (2011) Correlation of the apparent diffusion coefficient value and dynamic magnetic resonance imaging findings with prognostic factors in invasive ductal carcinoma. J Magn Reson Imaging JMRI 33:102–109. doi:10.1002/jmri.22400 CrossRefPubMed Jeh SK, Kim SH, Kim HS et al (2011) Correlation of the apparent diffusion coefficient value and dynamic magnetic resonance imaging findings with prognostic factors in invasive ductal carcinoma. J Magn Reson Imaging JMRI 33:102–109. doi:10.​1002/​jmri.​22400 CrossRefPubMed
29.
go back to reference Kim SH, Cha ES, Kim HS et al (2009) Diffusion-weighted imaging of breast cancer: correlation of the apparent diffusion coefficient value with prognostic factors. J Magn Reson Imaging JMRI 30:615–620. doi:10.1002/jmri.21884 CrossRefPubMed Kim SH, Cha ES, Kim HS et al (2009) Diffusion-weighted imaging of breast cancer: correlation of the apparent diffusion coefficient value with prognostic factors. J Magn Reson Imaging JMRI 30:615–620. doi:10.​1002/​jmri.​21884 CrossRefPubMed
31.
go back to reference Razek AAKA, Gaballa G, Denewer A, Nada N (2010) Invasive ductal carcinoma: correlation of apparent diffusion coefficient value with pathological prognostic factors. NMR Biomed 23:619–623. doi:10.1002/nbm.1503 CrossRefPubMed Razek AAKA, Gaballa G, Denewer A, Nada N (2010) Invasive ductal carcinoma: correlation of apparent diffusion coefficient value with pathological prognostic factors. NMR Biomed 23:619–623. doi:10.​1002/​nbm.​1503 CrossRefPubMed
33.
go back to reference De Felice C, Cipolla V, Guerrieri D et al (2014) Apparent diffusion coefficient on 3.0 Tesla magnetic resonance imaging and prognostic factors in breast cancer. Eur J Gynaecol Oncol 35:408–414PubMed De Felice C, Cipolla V, Guerrieri D et al (2014) Apparent diffusion coefficient on 3.0 Tesla magnetic resonance imaging and prognostic factors in breast cancer. Eur J Gynaecol Oncol 35:408–414PubMed
34.
go back to reference Kamitani T, Matsuo Y, Yabuuchi H et al (2013) Correlations between apparent diffusion coefficient values and prognostic factors of breast cancer. Magn Reson Med Sci 12:193–199CrossRefPubMed Kamitani T, Matsuo Y, Yabuuchi H et al (2013) Correlations between apparent diffusion coefficient values and prognostic factors of breast cancer. Magn Reson Med Sci 12:193–199CrossRefPubMed
35.
go back to reference Petralia G, Bonello L, Summers P et al (2011) Intraobserver and interobserver variability in the calculation of apparent diffusion coefficient (ADC) from diffusion-weighted magnetic resonance imaging (DW-MRI) of breast tumours. Radiol Med (Torino) 116:466–476. doi:10.1007/s11547-011-0616-z CrossRef Petralia G, Bonello L, Summers P et al (2011) Intraobserver and interobserver variability in the calculation of apparent diffusion coefficient (ADC) from diffusion-weighted magnetic resonance imaging (DW-MRI) of breast tumours. Radiol Med (Torino) 116:466–476. doi:10.​1007/​s11547-011-0616-z CrossRef
36.
go back to reference O’Flynn EAM, Morgan VA, Giles SL, deSouza NM (2012) Diffusion weighted imaging of the normal breast: reproducibility of apparent diffusion coefficient measurements and variation with menstrual cycle and menopausal status. Eur Radiol 22:1512–1518. doi:10.1007/s00330-012-2399-0 CrossRefPubMed O’Flynn EAM, Morgan VA, Giles SL, deSouza NM (2012) Diffusion weighted imaging of the normal breast: reproducibility of apparent diffusion coefficient measurements and variation with menstrual cycle and menopausal status. Eur Radiol 22:1512–1518. doi:10.​1007/​s00330-012-2399-0 CrossRefPubMed
38.
go back to reference Sharma U, Danishad KKA, Seenu V, Jagannathan NR (2009) Longitudinal study of the assessment by MRI and diffusion-weighted imaging of tumor response in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy. NMR Biomed 22:104–113. doi:10.1002/nbm.1245 CrossRefPubMed Sharma U, Danishad KKA, Seenu V, Jagannathan NR (2009) Longitudinal study of the assessment by MRI and diffusion-weighted imaging of tumor response in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy. NMR Biomed 22:104–113. doi:10.​1002/​nbm.​1245 CrossRefPubMed
Metadata
Title
MR mammography using diffusion-weighted imaging in evaluating breast cancer: a correlation with proliferation index
Authors
Cristina Molinari
Paola Clauser
Rossano Girometti
Anna Linda
Elisa Cimino
Fabio Puglisi
Chiara Zuiani
Massimo Bazzocchi
Publication date
01-10-2015
Publisher
Springer Milan
Published in
La radiologia medica / Issue 10/2015
Print ISSN: 0033-8362
Electronic ISSN: 1826-6983
DOI
https://doi.org/10.1007/s11547-015-0527-z

Other articles of this Issue 10/2015

La radiologia medica 10/2015 Go to the issue