Ultrasound high-definition microvasculature imaging with novel quantitative biomarkers improves breast cancer detection accuracy.
Breast cancer
Contrast-agent-free method
Neovascularization
Quantitative biomarkers
Ultrasound
Journal
European radiology
ISSN: 1432-1084
Titre abrégé: Eur Radiol
Pays: Germany
ID NLM: 9114774
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
received:
18
01
2022
accepted:
12
04
2022
revised:
24
03
2022
pubmed:
30
4
2022
medline:
19
11
2022
entrez:
29
4
2022
Statut:
ppublish
Résumé
To overcome the limitations of power Doppler in imaging angiogenesis, we sought to develop and investigate new quantitative biomarkers of a contrast-free ultrasound microvasculature imaging technique for differentiation of benign from malignant pathologies of breast lesion. In this prospective study, a new high-definition microvasculature imaging (HDMI) was tested on 521 patients with 527 ultrasound-identified suspicious breast masses indicated for biopsy. Four new morphological features of tumor microvessels, microvessel fractal dimension (mvFD), Murray's deviation (MD), bifurcation angle (BA), and spatial vascularity pattern (SVP) as well as initial biomarkers were extracted and analyzed, and the results correlated with pathology. Multivariable logistic regression analysis was used to study the performance of different prediction models, initial biomarkers, new biomarkers, and combined new and initial biomarkers in differentiating benign from malignant lesions. The new HDMI biomarkers, mvFD, BA, MD, and SVP, were statistically significantly different in malignant and benign lesions, regardless of tumor size. Sensitivity and specificity of the new biomarkers in lesions > 20 mm were 95.6% and 100%, respectively. Combining the new and initial biomarkers together showed an AUC, sensitivity, and specificity of 97% (95% CI: 95-98%), 93.8%, and 89.2%, respectively, for all lesions regardless of mass size. The classification was further improved by adding the Breast Imaging Reporting and Data System (BI-RADS) score to the prediction model, showing an AUC, sensitivity, and specificity of 97% (95% CI: 95-98%), 93.8%, and 89.2%, respectively. The addition of new quantitative HDMI biomarkers significantly improved the accuracy in breast lesion characterization when used as a complementary imaging tool to the conventional ultrasound. • Novel quantitative biomarkers extracted from tumor microvessel images increase the sensitivity and specificity in discriminating malignant from benign breast masses. • New HDMI biomarkers Murray's deviation, bifurcation angles, microvessel fractal dimension, and spatial vascularity pattern outperformed the initial biomarkers. • The addition of BI-RADS scores based on US descriptors to the multivariable analysis using all biomarkers remarkably increased the sensitivity, specificity, and AUC in all size groups.
Identifiants
pubmed: 35486168
doi: 10.1007/s00330-022-08815-2
pii: 10.1007/s00330-022-08815-2
pmc: PMC9616967
mid: NIHMS1803198
doi:
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7448-7462Subventions
Organisme : NCI NIH HHS
ID : R01 CA239548
Pays : United States
Organisme : NCI NIH HHS
ID : R01CA168575
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA015083
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA168575
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA195527
Pays : United States
Organisme : NCI NIH HHS
ID : R01CA239548
Pays : United States
Organisme : NCI NIH HHS
ID : R01CA195527
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
Nakamura Y, Yasuoka H, Tsujimoto M et al (2003) Flt-4-positive vessel density correlates with vascular endothelial growth factor-d expression, nodal status, and prognosis in breast cancer. Clin Cancer Res 9:5313–5317
Longatto Filho A, Lopes JM, Schmitt FC (2010) Angiogenesis and breast cancer. J Oncol 2010
Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407:249
doi: 10.1038/35025220
Nagy J, Chang S, Dvorak A, Dvorak H (2009) Why are tumour blood vessels abnormal and why is it important to know? Br J Cancer 100:865
doi: 10.1038/sj.bjc.6604929
Fukumura D, Duda DG, Munn LL, Jain RK (2010) Tumor microvasculature and microenvironment: novel insights through intravital imaging in pre-clinical models. Microcirculation 17:206–225
doi: 10.1111/j.1549-8719.2010.00029.x
Busilacchi P, Draghi F, Preda L, Ferranti C (2012) Has color Doppler a role in the evaluation of mammary lesions? J Ultrasound 15:93–98
doi: 10.1016/j.jus.2012.02.007
Chang Y-C, Huang Y-H, Huang C-S, Chang R-F (2012) Vascular morphology and tortuosity analysis of breast tumor inside and outside contour by 3-D power Doppler ultrasound. Ultrasound Med Biol 38:1859–1869
doi: 10.1016/j.ultrasmedbio.2012.06.010
Lee SW, Choi HY, Baek SY, Lim SM (2002) Role of color and power Doppler imaging in differentiating between malignant and benign solid breast masses. J Clin Ultrasound 30:459–464
doi: 10.1002/jcu.10100
Davoudi Y, Borhani B, Rad MP, Matin N (2014) The role of Doppler sonography in distinguishing malignant from benign breast lesions. J Med Ultrasound 22:92–95
doi: 10.1016/j.jmu.2013.12.001
Raza S, Baum JK (1997) Solid breast lesions: evaluation with power Doppler US. Radiology 203:164–168
doi: 10.1148/radiology.203.1.9122386
Yamaga I, Kawaguchi-Sakita N, Asao Y et al (2018) Vascular branching point counts using photoacoustic imaging in the superficial layer of the breast: a potential biomarker for breast cancer. Photoacoustics 11:6–13
doi: 10.1016/j.pacs.2018.06.002
Lee SC, Tchelepi H, Grant E et al (2019) Contrast-enhanced ultrasound imaging of breast masses: adjunct tool to decrease the number of false-positive biopsy results. J Ultrasound Med 38:2259–2273
doi: 10.1002/jum.14917
Du Y-R, Wu Y, Chen M, Gu X-G (2018) Application of contrast-enhanced ultrasound in the diagnosis of small breast lesions. Clin Hemorheol Microcirc 70:291–300
doi: 10.3233/CH-170368
Gessner RC, Aylward SR, Dayton PA (2012) Mapping microvasculature with acoustic angiography yields quantifiable differences between healthy and tumor-bearing tissue volumes in a rodent model. Radiology 264:733–740
doi: 10.1148/radiol.12112000
Gessner RC, Frederick CB, Foster FS, Dayton PA (2013) Acoustic angiography: a new imaging modality for assessing microvasculature architecture. J Biomed Imaging 2013:14
Errico C, Pierre J, Pezet S et al (2015) Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging. Nature 527:499
doi: 10.1038/nature16066
Opacic T, Dencks S, Theek B et al (2018) Motion model ultrasound localization microscopy for preclinical and clinical multiparametric tumor characterization. Nat Commun 9:1527
doi: 10.1038/s41467-018-03973-8
Shelton SE, Stone J, Gao F, Zeng D, Dayton PA (2020, 2020) Microvascular ultrasonic imaging of angiogenesis identifies tumors in a murine spontaneous breast cancer model. Int J Biomed Imaging
Christensen-Jeffries K, Couture O, Dayton PA et al (2020) Super-resolution ultrasound imaging. Ultrasound Med Biol 46:865–891
doi: 10.1016/j.ultrasmedbio.2019.11.013
Gong P, Song P, Huang C et al (2019) Ultrasensitive ultrasound microvessel imaging for characterizing benign and malignant breast tumors. Ultrasound Med Biol 45:3128–3136
doi: 10.1016/j.ultrasmedbio.2019.08.009
Park AY, Seo BK, Han M-R (2021) Breast ultrasound microvascular imaging and radiogenomics. Korean J Radiol 22:677
doi: 10.3348/kjr.2020.1166
X-y X, Chen X, Guan X-f WH, Qin W, Luo B-m (2016) Superb microvascular imaging in diagnosis of breast lesions: a comparative study with contrast-enhanced ultrasonographic microvascular imaging. Br J Radiol 89:20160546
doi: 10.1259/bjr.20160546
Bayat M, Fatemi M, Alizad A (2018) Background removal and vessel filtering of noncontrast ultrasound images of microvasculature. IEEE Trans Biomed Eng 66:831–842
doi: 10.1109/TBME.2018.2858205
Ghavami S, Bayat M, Fatemi M, Alizad A (2020) Quantification of morphological features in non-contrast-enhanced ultrasound microvasculature imaging. IEEE Access 8:18925–18937
doi: 10.1109/ACCESS.2020.2968292
Ternifi RWY, Polley EC, Fazzio RT, Fatemi M, Alizad A (2021) Quantitative biomarkers for cancer detection using contrast-free ultrasound high-definition microvessel imaging: fractal dimension, Murray’s deviation, bifurcation angle & spatial vascularity pattern. IEEE Trans Med Imaging Early Access:1–10
Bjaerum S, Torp H, Kristoffersen K (2002) Clutter filter design for ultrasound color flow imaging. IEEE Trans Ultrason Ferroelectr Freq Control 49:204–216
doi: 10.1109/58.985705
Sabo E, Boltenko A, Sova Y, Stein A, Kleinhaus S, Resnick MB (2001) Microscopic analysis and significance of vascular architectural complexity in renal cell carcinoma. Clin Cancer Res 7:533–537
Chen C, He Z-c, Shi Y et al (2018) Microvascular fractal dimension predicts prognosis and response to chemotherapy in glioblastoma: an automatic image analysis study. Lab Invest 98:924–934
doi: 10.1038/s41374-018-0055-2
Ziyrek M, Sertdemir AL, Duran M (2020) Effect of coronary artery bifurcation angle on atherosclerotic lesion localization distance to the bifurcation site. J Saudi Heart Assoc 32:399
doi: 10.37616/2212-5043.1071
Konerding M, Fait E, Gaumann A (2001) 3D microvascular architecture of pre-cancerous lesions and invasive carcinomas of the colon. Br J Cancer 84:1354–1362
doi: 10.1054/bjoc.2001.1809
Taber LA, Ng S, Quesnel AM, Whatman J, Carmen CJ (2001) Investigating Murray’s law in the chick embryo. J Biomech 34:121–124
doi: 10.1016/S0021-9290(00)00173-1
Secomb TW, Dewhirst MW, Pries AR (2012) Structural adaptation of normal and tumour vascular networks. Basic Clin Pharmacol Toxicol 110:63–69
doi: 10.1111/j.1742-7843.2011.00815.x
Caresio C, Caballo M, Deandrea M et al (2018) Quantitative analysis of thyroid tumors vascularity: a comparison between 3-D contrast-enhanced ultrasound and 3-D power Doppler on benign and malignant thyroid nodules. Med Phys 45:3173–3184
doi: 10.1002/mp.12971
Liu H, Jiang Y, Dai Q, Zhu Q, Wang L, Lu J (2014) Peripheral enhancement of breast cancers on contrast-enhanced ultrasound: correlation with microvessel density and vascular endothelial growth factor expression. Ultrasound Med Biol 40:293–299
doi: 10.1016/j.ultrasmedbio.2013.10.004
Mendelson EB, Berg WA, Merritt CR (2001) Toward a standardized breast ultrasound lexicon, BI-RADS: ultrasound. Seminars in Roentgenology. Elsevier, pp 217-225
Abdullah N, Mesurolle B, El-Khoury M, Kao E (2009) Breast imaging reporting and data system lexicon for US: interobserver agreement for assessment of breast masses. Radiology 252:665–672
doi: 10.1148/radiol.2523080670
Yongfeng Z, Ping Z, Wengang L, Yang S, Shuangming T (2016) Application of a novel microvascular imaging technique in breast lesion evaluation. Ultrasound Med Biol 42:2097–2105
doi: 10.1016/j.ultrasmedbio.2016.05.010
Kanoulas E, Butler M, Rowley C et al (2019) Super-resolution contrast-enhanced ultrasound methodology for the identification of in vivo vascular dynamics in 2D. Invest Radiol 54:500
doi: 10.1097/RLI.0000000000000565
Sun M, Lv W, Zhao X et al (2020) Vascular branching geometry relating to portal hypertension: a study of liver microvasculature in cirrhotic rats by X-ray phase-contrast computed tomography. Quant Imaging Med Surg 10:116
doi: 10.21037/qims.2019.11.04
Xuan R, Zhao X, Jian J et al (2019) Phase-contrast computed tomography: a correlation study between portal pressure and three dimensional microvasculature of ex vivo liver samples from carbon tetrachloride-induced liver fibrosis in rats. Microvasc Res 125:103884
doi: 10.1016/j.mvr.2019.103884
Chen X, Dai J, Lin J et al (2020) Image-based morphometric studies of human coronary artery bifurcations with/without coronary artery disease. Comput Methods Biomech Biomed Engin:1–17
Schoenenberger AW, Urbanek N, Toggweiler S et al (2012) Deviation from Murray’s law is associated with a higher degree of calcification in coronary bifurcations. Atherosclerosis 221:124–130
doi: 10.1016/j.atherosclerosis.2011.12.040
Murray CD (1926) The physiological principle of minimum work applied to the angle of branching of arteries. J Gen Physiol 9:835–841
doi: 10.1085/jgp.9.6.835
Grunstein J, Masbad JJ, Hickey R, Giordano F, Johnson RS (2000) Isoforms of vascular endothelial growth factor act in a coordinate fashion to recruit and expand tumor vasculature. Mol Cell Biol 20:7282–7291
doi: 10.1128/MCB.20.19.7282-7291.2000
Ferrara KW, Merritt CR, Burns PN, Foster FS, Mattrey RF, Wickline SA (2000) Evaluation of tumor angiogenesis with US: imaging, Doppler, and contrast agents. Acad Radiol 7:824–839
doi: 10.1016/S1076-6332(00)80631-5
Tozer GM, Akerman S, Cross NA et al (2008) Blood vessel maturation and response to vascular-disrupting therapy in single vascular endothelial growth factor-A isoform–producing tumors. Cancer Res 68:2301–2311
doi: 10.1158/0008-5472.CAN-07-2011
Bullitt E, Zeng D, Gerig G et al (2005) Vessel tortuosity and brain tumor malignancy: a blinded study1. Acad Radiol 12:1232–1240
doi: 10.1016/j.acra.2005.05.027
Chappell JC, Wiley DM, Bautch VL (2012) How blood vessel networks are made and measured. Cells Tissues Organs 195:94–107
doi: 10.1159/000331398
Uzzan B, Nicolas P, Cucherat M, Perret G-Y (2004) Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 64:2941–2955
doi: 10.1158/0008-5472.CAN-03-1957
Rykala J, Przybylowska K, Majsterek I et al (2011) Angiogenesis markers quantification in breast cancer and their correlation with clinicopathological prognostic variables. Pathol Oncol Res 17:809–817
doi: 10.1007/s12253-011-9387-6
Demené C, Tiran E, Sieu L-A et al (2016) 4D microvascular imaging based on ultrafast Doppler tomography. Neuroimage 127:472–483
doi: 10.1016/j.neuroimage.2015.11.014
Flesch M, Pernot M, Provost J et al (2017) 4D in vivo ultrafast ultrasound imaging using a row-column addressed matrix and coherently-compounded orthogonal plane waves. Phys Med Biol 62:4571
doi: 10.1088/1361-6560/aa63d9
Rizzo S, Botta F, Raimondi S et al (2018) Radiomics: the facts and the challenges of image analysis. Eur Radiol Exp 2:36
doi: 10.1186/s41747-018-0068-z
Gillies RJ, Kinahan PE, Hricak H (2015) Radiomics: images are more than pictures, they are data. Radiology 278:563–577
doi: 10.1148/radiol.2015151169
Goldhirsch A, Wood WC, Coates AS et al (2011) Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 22:1736–1747
doi: 10.1093/annonc/mdr304